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Preparation, structure and antimicrobial properties of modified gelatin composite hydrogel from chicken, bovine and porcine lung

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  • In this paper, the reaction process parameters of the hydrogel produced by the modified gelatin from chicken, bovine and porcine lungs with carboxymethyl chitosan (CMCS) and oxidized glucomannan (OKGM) were optimized to produce Schiff base reaction. The results showed the properties of the three composite hydrogels are improved when the value of gelatin/CMCS/OKGM reached 1:2:2. The best modified gelatin/CMCS/OKGM of bovine lung composite hydrogel (COBH) had a gelatin strength of 8.14 N, a swelling rate of 257%, a water evaporation rate of 66.86%, and an antibacterial property of 38.02%. The properties of modified gelatin/CMCS/OKGM of chicken lung composite hydrogel (COCH) were similar to those of COBH. However, the water holding capacity of COCH was higher than that of COBH. The properties of the modified gelatin/CMCS/OKGM for porcine lung composite hydrogel (COPH) were significantly decreased over those of the other two. Therefore, COCH has potential applications in food coating and preservation.
  • Agricultural management practices impact soil physicochemical properties to a remarkable extent. Degradation of soil health has led to a contraction in agricultural production and soil biodiversity particularly due to conventional farming practices, indiscriminate use of inorganic fertilizers (INF) and inadequate input of residues[1]. Organic or inorganic fertilizers have been regarded as a critical component of agriculture to accomplish global food security goals[2]. The exogenous supply of fertilizers could easily alter soil properties by restoring the nutrients that have been absorbed by the plants[2]. Thus, implementing adequate nutrient management strategies could boost plant yield and sustain plant health. Tillage affects the soil, especially for crop production and consequently affects the agro-ecosystem functions. This involves the mechanical manipulation of the soil to modify soil attributes like soil water retention, evapotranspiration, and infiltration processes for better crop production. Thus, tillage practices coupled with fertilizer inputs may prove a viable strategy to improve soil health components such as nutrient status, biodiversity, and organic carbon.

    Soil serves as a major reservoir of nutrients for sustainable crop production. Intensive cultivation due to growing population burden has led to the decline of soil nutrient status that has adversely affected agricultural production. Various researchers have assessed the soil nutrient budget and the reasons behind decline of nutrient content in soil[3]. Soil management strategies have assisted in overcoming this problem to a greater extent. Tillage practices redistribute soil fertility and improve plant available nutrient content due to soil perturbations[4]. Different tillage and fertilization practices alter soil nutrient cycling over time[5]. Fertilization is an important agricultural practice which is known to increase nutrient availability in soil as well as plants[6]. A report has been compiled by Srivastava et al.[7], which assessed the effectiveness of different fertilizers on soil nutrient status in Indian soils.

    Soil biota has a vital role in the self-regulating functions of the soil to maintain soil quality which might reduce the reliance on anthropogenic activities. Soil microbial activities are sensitive to slight modifications in soil properties and could be used as an index of soil health[8]. Maintenance of microbial activity is essential for soil resilience as they influence a diverse range of parameters and activities including soil structure formation, soil SOM degradation, bio-geochemical cycling of nutrients etc.[9]. Various researchers have identified microbial parameters like microbial biomass carbon (MBC), potentially mineralizable nitrogen (PMN), soil respiration, microbial biomass nitrogen (MBN), and earthworm population as potential predictors of soil quality. Geisseler & Scow[10] have compiled a review on the affirmative influence of long-term mineral fertilization on the soil microbial community.

    Being the largest terrestrial carbon (C) reservoir, soil organic carbon (SOC) plays a significant role in agricultural productivity, soil quality, and climate change mitigation[11]. Manure addition, either solely or along with INF augments SOC content which helps in the maintenance and restoration of SOM more effectively as compared to the addition of INF alone[12]. Enhancement of recalcitrant and labile pools of SOC could be obtained through long-term manure application accentuating the necessity of continuous organic amendments for building up C and maintaining its stability[13]. Generally, compared with manure addition, INF application is relatively less capable of raising SOC and its labile fractions[14]. Alteration in SOC content because of management strategies and/or degradation or restoring processes is more prominent in the labile fraction of soil C[15]. Several fractions of soil C play vital roles in food web and nutrient cycles in soils besides influencing many biological properties of soil[16]. Thus, monitoring the response of SOC and its fractions to various management practices is of utmost importance.

    A positive impact on SOC under manure application coupled with INF in rice-wheat systems has been reported, as compared to sole applications of INFs[17]. Although ploughing and other mechanical disturbances in intensive farming cause rapid OM breakdown and SOC loss[18], additional carbon input into the soil through manure addition and rational fertilization increases carbon content[13]. Wei et al.[19] in light sandy loam soil of China found that the inclusion of crop straw together with inorganic N, P and K fertilizers showed better results for improving soil fertility over sole use of inorganic fertilizers. Zhu et al.[20] studied the influence of soil C through wheat straw, farmyard manure (FYM), green manure, and rice straw on plant growth, yield, and various soil properties and found that the recycling of SOM under intensive cultivation is completely reliant on net OM input and biomass inclusion. However, most of the studies on residue management and organically managed systems could not provide clear views regarding the relations between the quality of OM inputs and biological responses towards it. The disintegration of soil aggregates due to ploughing, use of heavy machinery, and residue removal has been reported widely under conventional tillage (CT) practices[21]. On the contrary, improvement in SOC stabilization has also been observed by some scientists[22]. Under CT, the disintegration of macro-aggregates into micro-aggregates is a prominent phenomenon, while conservation tillage has been identified as a useful practice for increasing macro-aggregates as well as carbon sequestration in agricultural soils[23]. By and large, the ploughing depth (0–20 cm) is taken into consideration for evaluating the impact of tillage and straw retention on soil aggregation[24], while degradation in deeper layers of soil is becoming a major constraint towards soil quality together with crop yield[25].

    Hence, the present review would be useful in determining how tillage practices and inorganic and organic fertilization impact nutrient availability in the soil, microbial composition and SOC fractions besides stocks under different land uses.

    Agricultural production is greatly influenced by nutrient availability and thus nutrient management is required for sustaining higher yields of crop. The term 'nutrient availability' refers to the quantity of nutrients in chemical forms accessible to plant roots or compounds likely to be converted to such forms throughout the growing season in lieu of the total amount of nutrients in the soil. For optimum growth, different crops require specifically designed nutrient ratios. Plants need macronutrients [nitrogen (N), phosphorus (P), potassium (K) in higher concentrations], secondary nutrients [calcium (Ca), magnesium (Mg), sulphur (S) in moderate amounts as compared to macronutrients] and Micronutrients [Zn (zinc), Fe (iron), Cu (copper), B (boron), Mn (manganese), Mo (molybdenum) in smaller amounts] for sustainable growth and production[26]. Fertilizers assist the monitoring of soil nutrient levels by direct addition of required nutrients into the soil through different sources and tillage practices may alter the concentration of available plant nutrients through soil perturbations. Various studies on the influence of fertilization and tillage practices on available plant nutrients have been discussed below.

    Yue et al.[27] reported that long-term fertilization through manure/INF improved the macronutrient content of Ultisol soil in China. Two doses of NPK (2NPK) considerably improved soil properties over a single dose (NPK). Combined application (NPK + OM) resulted in higher hydrolysable N and available P over the sole OM application. The total K content was higher under the treatments NPK, 2NPK and NPK + OM than sole OM treatment, whereas available K was higher in treatments NPK + OM and 2NPK over the sole OM and NPK. Likewise, OM, INF, and OM + INF were evaluated for their potential to regulate the soil macronutrient dynamics. Organic manure significantly improved the soil N content, whereas INF showed comparable results to that of the control treatment. Besides, all the treatments improved available P and exchangeable K concentration[28].

    Hasnain et al.[29] performed comparative studies of different ratios of INF + compost and different application times for the chemical N fertilizer on silty loamy soils of China. The available nitrogen and phosphorous content were greater in conjoint OM + INF application over the bare INF and control application irrespective of N application time. Soil quality substantially improved with increasing ratio of compost and 70:30 (INF to compost ratio) was found to be most suitable to maintain soil fertility and nutrient status. Another study by Liu et al.[30] reported the superior effects of NPK + pig manure and NPK + straw to improve soil available P and K over the control and sole NPK treatments. However, total N concentration did not exhibit any significant variation under any treatment.

    Shang et al.[31] accounted the positive impact of vermicompost and mushroom residue application on grassland soil fertility in China. The addition of organic manures improved available P and K content to a considerable extent. Under moisture-deficit winter wheat-fallow rotation, another study quantified the influence of residue management approaches and fertilizer rate on nutrient accrual. Residue burning resulted in no decline in soil macronutrient content, whereas the perpetual addition of FYM for 84 years significantly improved total N and extractable K and P concentration. Thus, residue incorporation along with FYM application may prove beneficial in reducing the temporal macronutrient decline[32].

    Ge et al.[33] examined the effects of NPK and NPK along with manure (NPKM) addition on the macronutrient status of Hapli-Udic Cambisol soil. The NPKM application resulted in the highest increase in total N, available-P and K concentration as compared to NPK and control. Likewise, mineral fertilization reduction and partial substitution with organic amendments have posed a significant influence on soil macronutrient status. Soil available P and K decreased after INF reduction[34]. Chen et al.[35] evinced that integrated application of manure and mineral fertilizers to red clay soil (typical Ultisols) improved hydrolyzed nitrogen and available P due to an increase in the decomposition of organic matter (OM) and N bio-fixation than sole mineral fertilizers and control.

    A long-term experiment was carried out out by Shiwakoti et al.[36] to ascertain the influence of N fertilization and tillage on macronutrient dynamics in soil. Nitrogen fertilization produced higher crop biomass which might have improved total N and P concentration in soil. Moreover, the reduced interaction between soil colloids and residue or greater cation exchange sites due to tillage practices could have augmented K concentration in 0−10 cm soil depth. Likewise, among tillage systems combined organic (poultry manure) and inorganic (lime and fertilizers) fertilization, no-tillage, and reduced tillage with organic fertilization resulted in higher availability of P owing to minimal disturbance of soil which decreases contact surface between phosphate ions and adsorption sites. Greater losses of K in runoff water under NT resulted in lower K availability under NT than CT[37].

    The influence of tillage systems on soil nutrient dynamics showed that minimal soil disturbances under zero tillage prohibited redistribution of soil nutrients and resulted in the highest available N, P, and K in the surface soil[38]. The influence of tillage timing on soil macronutrient status has also been assessed under tillage treatments that are fall tillage (FT), spring tillage (ST), no tillage (NT), and disk/chisel tillage (DT/CT) on mixed mesic Typic Haploxerolls soil. All the tillage systems differed in the quantity of residues generated. Thus, variation in the decomposition of crop residue and mineralization of SOM resulted in variable rates of nutrient release. The FT and ST had the highest N content over DT/CT and NT systems at corresponding depth. The N content also decreased with soil depth irrespective of tillage treatment. The available P and extractable K were highest under NT at the top 10 cm soil depth and increased over time[39]. Residue management in combination with tillage treatments (ST and CT) has been reported to affect the soil macronutrient status in Bangladesh. Tillage treatments enhanced the total N content to a considerable extent. Moreover, 3 years of residue retention led to a higher concentration of total N, available P and K in the soil.

    The combinations of N, P, and K in different ratios together with two rates of organic fertilizer (OF) applied on the aquic Inceptisol having sandy loam texture influenced the micronutrient status of the soil[40]. Soil Zn content decreased with time when no fertilizer was applied as compared to organic fertilizer (OF) application. The mineral fertilizer treatments led to a substantial increase in DTPA-extractable micronutrients in the soil. The higher micronutrient concentration due to higher OM highlights the importance of maintaining OM for soil fertility and higher crop production. Further studies revealed that long-term application of sole N fertilizers led to a significant decline in total Zn and Cu, whereas Mn and Fe status improved through atmospheric deposition. Phosphorus and OF addition along with straw incorporation markedly increased total Zn, Cu, Fe, and Mn. The DTPA-extractable Mn, Zn, Fe, and Cu were also higher in OF treatment, thus demonstrating the beneficial effects of constant OM application for maintaining the nutrient status of soil[41].

    López-Fando & Pardo[42] quantified the impact of various tillage practices including NT, CT, minimum tillage (MT), and zone-tillage (ZT) on soil micronutrient stocks. Tillage systems did exhibit a significant influence on plant available Fe stocks in the topsoil; however, diminished with depth under ZT, NT and MT. Manganese was higher in NT and ZT at all depths and increased with soil depth. Zinc was highest under NT and other results did not vary significantly as in the case of Cu. The SOC levels were also found to be responsible to affect micronutrients due to tillage practices. Likewise, in Calciortidic Haploxeralf soil the distribution of soil micronutrients (Zn, Mn, Fe, Cu) was ascertained under different tillage practices (CT, MT, and NT). The micronutrient status was highest under NT in the upper layers due to the higher SOC level[43].

    Sharma & Dhaliwal[44] determined that the combined application of nitrogen and rice residues facilitated the transformation of micronutrients (Zn, Mn, Fe, Cu). Among different fractions, the predominant fractions were crystalline Fe bound in Zn, Mn, and Cu and amorphous Fe oxide in Fe with 120 kg N ha˗1 and 7.5-ton rice residue incorporation. The higher content of occluded fractions adduced the increment in cationic micronutrient availability in soil with residue incorporation together with N fertilization due to increased biomass. Rice straw compost along with sewage sludge (SS) and INF also affected the micronutrient availability under the RW cropping system. Nitrogen fertilization through inorganic fertilizers and rice straw compost and sewage sludge (50% + 50%) improved soil micronutrient status due to an increase in SOM over sole NPK fertilizers[45]. Earlier, Dhaliwal et al.[46] in a long-term experiment determined that different combinations of NPK along with biogas slurry as an organic source modified the extractable micronutrient status of the soil.

    A comparative study was carried out by Dhaliwal et al.[47] to ascertain the long-term impact of agro-forestry and rice–wheat systems on the distribution of soil micronutrients. The DTPA-extractable and total Cu, Zn, Fe, and Mn were greater in the RW system due to the reduced conditions because of rice cultivation. Under the RW system Zn removal was higher which was balanced by continuous Zn application. The higher availability of Fe under the RW system was due to reduced conditions. Contrarily, Mn was greater under the agro-forestry system owing to nutrient recycling from leaf litter.

    The long-term impact of integrated application of FYM, GM, WCS (wheat-cut straw) and INF on the soil micronutrients (Zn, Mn, Cu, and Fe) have been studied by Dhaliwal et al.[48]. The FYM application substantially improved DTPA-extractable Zn status followed by GM and WCS, whereas Cu content was maximum in the plots with OM application. The highest Fe concentration was recorded in treatment in which 50% recommended N supplied through FYM. This could be ascribed to the release of micronutrients from OM at low soil pH.

    Shiwakoti et al.[49] studied the dual effects of tillage methods (MP, DP, SW) and variable rates of N (0, 45, 90, 135 and 180 kg ha−1) on the distribution of micronutrients under a moisture-deficit winter wheat-fallow system. The soil Mn content was highest under the DP regime. Inorganic N application reduced Cu content in the soil. Comparative studies with adjacent undisturbed grass pasture indicated the loss of Zn and Cu to a significant extent. Thus, DP along with nitrogen added through inorganic fertilizers could improve micronutrient concentration in the soil. Moreover, the results implied that long-term cultivation with nitrogen fertilization and tillage results in the decline of essential plant nutrients in the soil. Thus, organic amendments along with INF may prove an effective approach to increase soil micronutrient content. In another study conducted by Lozano-García & Parras-Alcántara[50] tillage practices such as NT under apple orchard, CT with the wheat-soybean system and puddling (PD) in the rice-rice cropping system were found to affect nutrient status. Under CT, Cu content was lowest and Zn content was highest. On the contrary, puddling caused an increase in Fe and Mn concentration owing to the dispersion of soil aggregates which reduced the percolation of water and created an anaerobic environment thereby enhancing the availability of Fe and Mn.

    Tillage practices along with gypsum fertilization have been known to affect secondary nutrient concentrations in soil. In a long-term experiment, FYM application showed maximum response to increased S concentration due to the maximum addition of OM through FYM over other treatments as S is an essential component of OM and FYM[32]. Higher Mg content was recorded in FYM and pea vine treatments because the application of organic matter through organic manure or pea vines outright led to Mg accrual. The lower Mg concentration in topsoil than the lower layers was due to the competition between Mg and K for adsorbing sites and thus displacement of Mg by K. Han et al.[28] while ascertaining the impact of organic manures and mineral fertilizers (NPK) on soil chemical attributes determined that INF application reduced exchangeable calcium, whereas no significant changes were exhibited in the magnesium concentrations. The OM application significantly increased both the calcium and magnesium concentrations in the soil.

    While ascertaining the effect of different tillage treatments such as CT, NT, and MT on exchangeable and water-soluble cations, Lozano-García & Parras-Alcántara[50] recorded that NT had greater content of exchangeable Ca2+ and Mg2+ than MT and CT. The exchangeable Ca2+ decreased with depth, however, opposite results were observed for Mg2+ which might be due to the higher uptake of Mg2+ by the crop. On another note, there might be the existence of Mg2+-deficient minerals on the surface horizon. Alam et al.[51] studied the temporal effect of tillage systems on S distribution in the soil and observed that available S was 19%, 31%, and 34% higher in zero tillage than in minimum tillage, conventional tillage, and deep tillage, respectively.

    Kumar et al.[38] appraised the impact of tillage systems on surface soil nutrient dynamics under the following conditions: conventional tillage, zero till seeding with bullock drawn, conventional tillage with bullock drawn seeding, utera cropping and conservation tillage seeding with country plough and observed that tillage had a significant impact on the available S content. Compared with conventional tillage, zero and minimum tillage had higher S content as there was none or limited tillage operations which led to the accumulation of root stubble in the soil that decomposed over time and increased S concentration.

    Soil is considered a hotspot for microbial biodiversity which plays an important role in building a complex link between plants and soil. The microbial components exhibit dynamic nature and, therefore, are characterized as good indicators of soil quality[52]. These components include MBC, MBN, PMN and microbial respiration which not only assist in biological transformations like OM conversion, and biological nitrogen fixation but also increase nutrient availability for crop uptake. Management strategies such as fertilizer inputs and tillage practices may exert beneficial effects on soil biota as discussed below.

    Soil is an abode to a considerable portion of global biodiversity. This biodiversity not only plays a pivotal role in regulating soil functions but also provides a fertile ground for advancing global sustainability, especially agricultural ventures. Thus, the maintenance of soil biodiversity is of paramount importance for sustaining ecosystem services. Soil biodiversity is the diverse community of living creatures in the soil that interact not only with one another but also with plants and small animals to regulate various biological activities[53]. Additionally, it increases the fertility of soil by converting organic litter to SOM thereby enhancing SOC content. Thus, the SOM measures the number and activity of soil biota. Furthermore, the quality and amount of SOC, as well as plant diversity have a considerable impact on the soil microbial community structure[54].

    Dangi et al.[55] ascertained the impact of integrated nutrient management and biochar on soil microbial characteristics and observed that soil amended with biochar or the addition of organic manures influenced microbial community composition and biomass and crop yield. After two years, the higher rates of biochar significantly enhanced the levels of gram-positive and gram-negative bacterial phospholipid fatty acid (PLFA), total arbuscular mycorrhizal fungal (AMF) than lower rates, unfertilized and non-amended soil. Luan et al.[56] conducted a comparison study in a greenhouse to assess the effects of various rates of N fertilizer and kinds (inorganic and organic) on enzyme activities and soil microbial characteristics. Microbial growth (greater total PLFAs and microbial biomass carbon) and activity were promoted by manure substitution of mineral fertilizer, particularly at a higher replacement rate. On account of lower response in bacterial over fungal growth, manure addition led to a greater fungi/bacteria ratio. Furthermore, manure application significantly enhanced microbial communities, bacterial stress indicators and functional diversity. Lazcano et al.[57] determined the influence of different fertilization strategies on microbial community structure and function, soil biochemical properties and crop yield three months after addition of fertilizer. The integrated fertilizer regimes augmented microbial growth with improved enzyme activity as compared to sole inorganic amendments. Bacterial growth showed variable response with variation in fertilizer regime used whereas fungal growth varied with the amount of fertilizer added. Compared to mineral fertilizers, manure application led to a rapid increase in PLFA biomarkers for gram-negative bacteria. The organic amendments exhibited significant effects even at small concentration of the total quantity of nutrients applied through them; thus, confirming the viability of integrated fertilizer strategies in the short term.

    Kamaa et al.[58] assessed the long-term effect of crop manure and INF on the composition of microbial communities. The organic treatments comprised of maize (Zea mays) stover (MS) at 10 t ha−1 and FYM @ 10 t ha−1, INF treatments (120 kg N, 52.8 kg P-N2P2), integrated treatments (N2P2 + MS, N2P2 + FYM), fallow plot and control. The treatment N2P2 exhibited unfavourable effects on bacterial community structure and diversity that were more closely connected to the bacterial structure in control soils than integrated treatments or sole INF. In N2P2, fungal diversity varied differently than bacterial diversity but fungal diversity was similar in the N2P2 + FYM and N2P2 + MS-treated plots. Thus, the total diversity of fungal and bacterial communities was linked to agroecosystem management approaches which could explain some of the yield variations observed between the treatments. Furthermore, a long-term experiment was performed by Liu et al.[59] to study the efficiency of pig manure and compost as a source for N fertilization and found unique prokaryotic communities with variable abundance of Proteobacteria under compost and pig manure treatments.

    Recently, Li et al.[60] assessed the influence of different tillage practices (no-tillage, shallow tillage, deep tillage, no-tillage with straw retention, shallow tillage with straw retention and deep tillage with straw retention) on microbial communities and observed that tillage practices improved the bacterial Shannon index to a greater extent over the no-tillage plots in which the least value was recorded. Another research study by He et al.[61] reported the effect of tillage practices on enzyme activities at various growth stages. Across all the growth stages, enzyme activities of cellobiohydrolase (CBH), β-xylosidase (BXYL), alkaline phosphatase (AP), β-glucosidase (BG), β-N-acetylglucosamines (NAG) were 17%−169%, 7%−97%, 0.12%−29%, 3%−66%, 23%−137% greater after NT/ST, NT, ST, ST/PT, and PT/NT treatments as compared to plow tillage. The NT/ST treatment resulted in highest soil enzyme activities and yield, and thus was an effective and sustainable method to enhance soil quality and crop production.

    Microbes play a crucial role in controlling different soil functions and soil ecology and microbial community show significant variation across as well as within the landscape. On average, the total biomass of microbes exceeds 500 mg C kg soil−1[62]. Microbial biomass carbon is an active constituent of SOM which constitutes a fundamental soil quality parameter because SOM serves as a source of energy for microbial processes and is a measure of potential microbial activity[48,63]. Soil systems that have higher amounts of OM indicate higher levels of MBC. Microbial biomass carbon is influenced by many parameters like OM content in the soil, land use, and management strategies[64]. The MBC and soil aggregate stability are strongly related because MBC integrates soil physical and chemical properties responds to anthropogenic activities.

    Microbial biomass is regarded as a determinative criterion to assess the functional state of soil. Soils having high functional diversity of microbes which, by and large, occurs under organic agricultural practices, acquire disease and insect-suppressive characteristics that could assist in inducing resistance in plants[65]. Dou et al.[66] determined that soil microbial biomass C (SMBC) was 5% to 8% under wheat-based cropping systems and zero tillage significantly enhanced SMBC in the 0−30 cm depth, particularly in the upper 0 to 5 cm. According to Liang et al.[67], SMBC and soil microbial biomass N (SMBN) in the 0−10 cm surface layer were greater in the fertilized plots in comparison to the unfertilized plots on all sampling dates whereas microbial biomass C and N were highest at the grain filling stage. Mandal et al.[68] demonstrated that MBC also varied significantly with soil depth. Surface soil possessed a maximum MBC value than lower soil layers due to addition of crop residues and root biomass on the surface soil. The MBC content was highest with combined application of INF along with farmyard manure and GM, whereas untreated plots showed minimum MBC values. The incorporation of CR slows down the rate of mineralization processes; therefore, microbes require more time to decompose the residues and utilize the nutrients released[69]. On the other hand, incorporation of GR having a narrow C:N ratio enhances microbial activity and consequently accelerates mineralization in the soil. Malviya[70] also recorded that the SMBC contents were significantly greater under RT than CT, regardless of soil depth which was also assigned to residue incorporation which increases microbial biomass on account of higher carbon substrate in RT.

    Naresh et al.[71] studied the vertical distribution of MBC under no-tillage (NT), shallow (reduced) tillage and normal cultivated fields. A shallow tillage system significantly altered the tillage induced distribution of MBC. In a field experiment, Nakhro & Dkhar[72] examined the microbial populations and MBC in paddy fields under organic and inorganic farming approaches. The organic source used was a combination of rock phosphate, FYM and neem cake, whereas a mixture of urea, muriate of potash and single super phosphate was used as an inorganic source. The organically treated plots exhibited the highest MBC compared to inorganically treated plots and control. Organic carbon exhibited a direct and significant correlation with bacterial and fungal populations. The addition of organic fertilizers enhanced the content of SOC and consequently resulted in higher microbial count and MBC. Ramdas et al.[73] investigated the influence of inorganic and organic sources of nutrients (as minerals or INF) applied over a five-year period on SOC, MBC and other variables. It was observed that the addition of FYM and conjoint application of paddy straw (dry) and water hyacinth (PsWh) (fresh) significantly increased the SOC content than vermicompost, Chromolaena adenophorum (fresh) and Glyricidia aculeate (fresh), and Sesbania rostrata (fresh).

    Xu et al.[74] evaluated the influence of long-term fertilization strategies on the SOC content, soil MBN, soil MBC, and soil microbial quotient (SMQ) in a continuous rice system and observed that MBC at the main growth stages of early and late rice under 30% organic matter and 70% mineral fertilizer and 60% organic matter and 40% mineral fertilizer treatments was greater as compared to mineral fertilizer alone (MF), rice straw residues and mineral fertilizer (RF), and no fertilizer (CK) treatments. However, SMBC levels at late growth stages were greater in comparison to early growth stages. A recent study by Xiao et al.[75] demonstrated that increasing tillage frequency (no-tillage, semi-annual tillage, and tillage after every four months, two months, and one month) decreased soil MBC. Microbial biomass carbon content was significantly greater in no-till treatment (597 g kg−1) than in tillage every four months (421 g kg−1), two months (342 g kg−1) and one month (222 g kg−1). The decrease in the content of MBC in association with tillage practices is due to soil perturbations which enhanced soil temperature, diminished soil moisture content, and resulted in the destruction of microbial habitat and fungal hyphae. Therefore, the MBC content eventually affected the N cycle.

    Li et al.[76] reported that in comparison to CT, NT and RT resulted in increased MBC content and NT significantly increased MBC by 33.1% over CT. Furthermore, MBC concentration was 34.1% greater in NT than RT. The increase in MBC concentration was correlated with the results of increase in SOC concentration. Site-specific factors including soil depth and mean annual temperature significantly affected the response ratio of MBC under NT as compared to the duration of NT.

    Microbial biomass nitrogen (MBN) is a prominent indicator of soil fertility as it quantifies the biological status of soil. Soil MBN is strongly associated with organic matter of the soil. The nitrogen in MBN has a rapid turnover rate thereby reflecting the changes in management strategies way before the transformations in total N are discernable[77].

    In an experiment on continuous silage maize cultivation with crop rotation, Cerny et al.[78] observed that organic fertilizers exerted an affirmative influence on the soil MBN. During the application of organic manure MBN decreased, but there was higher MBN content as compared to control. However, addition of mineral nitrogenous fertilizers exerted an adverse effect on MBN content in experiments with maize. El-Sharkawi[79] recorded that organic matter-treated pots resulted in maximum MBN content than urea-treated pots. The sludge application enhanced total MBN and, therefore, could implicitly benefit crop production particularly in poor soils[18]. Sugihara et al.[80] observed that during the grain-filling stage in maize, residue and/or fertilizer addition exerted a pronounced influence on soil microbial dynamics; however, a clear effect of residue and ⁄or fertilizer addition was not observed. Microbial biomass nitrogen reduced dramatically from 63–71 to 18–33 kg N ha˗1 and C:N ratio at the same time increased more than ten-fold in all plots.

    Malik et al.[81] apprised that the organic amendments significantly enhanced MBN concentrations up to 50% more than the unamended soil. Wang et al.[82] evaluated the influence of organic materials on MBN content in an incubation and pot experiment with acidic and calcareous soils. The results revealed that MBN content which was affected by the different forms of organic amendments, increased by 23.37%−150.08% and 35.02%−160.02% in acidic and calcareous soils, respectively. The MBN content of both soils decreased with the increase in the C/N ratio of the organic materials, though a higher C/N ratio was effective for sustaining a greater MBN content for a very long time.

    Dhaliwal & Bijay-Singh[52] observed higher MBN levels in NT soils (116 kg ha−1) than in cultivated soils (80 kg ha−1). Kumar et al.[83] ascertained that in surface layer, MBN content was 11.8 mg kg−1 in CT which increased to 14.1 and 14.4 mg kg−1 in ZT and RT without residue retention and 20.2, 19.1 and 18.2 mg kg−1 in ZT, RT and CT with residue incorporation, respectively (Table 1). In the subsurface layer, the increased tendency on account of tillage and crop residue retention was identical to those of 0−15 cm layer but the magnitude was comparatively meagre (Table 1). In comparison to control, the persistent retention of crop residues led to significant accrual of MBN in the surface layer.

    Table 1.  Effect of different treatments on contents of various fractions of soil organic carbon[38].
    TreatmentsPMN (mg kg−1)MBC (mg kg−1)MBN (mg kg−1)DOC (mg kg−1)
    Depths (cm)
    0−1515−300−1515−300−1515−300−1515−30
    Tillage practices
    ZTR12.411.2562.5471.120.218.9198.6183.6
    ZTWR8.57.6350.4302.114.112.6167.1159.2
    RTR10.69.9490.2399.319.117.2186.4171.6
    RTWR7.66.6318.1299.814.413.7159.5148.7
    CTR9.38.5402.9354.418.216.6175.9168.9
    CT6.75.6307.9289.511.89.7142.5134.6
    Nitrogen management
    Control3.62.8218.3202.910.810.4103.792.3
    80 kg N ha−15.34.4241.1199.414.912.2128.3116.9
    120 kg N ha−18.97.6282.7220.916.516.1136.8123.6
    160 kg N ha−19.88.4343.9262.919.418.1164.8148.9
    200 kg N ha−110.49.7346.3269.622.721.7155.7136.4
    ZTR = Zero tillage with residue retention, ZTWR = Zero tillage without residue retention; RTR = Reduced tillage with residue retention, RTWR = Reduced tillage without residue retention, CTR = Conventional tillage with residue incorporation; CT = Conventional tillage without residue incorporation.
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    Xiao et al.[75] determined that the MBN content decreased with tillage treatment having highest value in no tillage treatment, however, the difference among the treatments was negligible. Soil perturbations decreased the aggregate size and thus lower the soil aeration and exposure of fresh organic matter which restricted the growth of microorganisms. The results also concluded that MBN content is highly sensitive to tillage. Ginakes et al.[84] assessed the impact of zone tillage intensity on MBN in a corn-kura clover cropping sequence. Microbial biomass nitrogen was influenced by time and type of tillage treatment. Temporal studies revealed that MBN was higher after tillage treatment than the values possessed before tillage. Under different tillage treatments, higher values were recorded in ST (shank-till) and DT (double-till) over NT and RZT (zone-till) treatments.

    Another biological parameter, PMN, is a crucial parameter of soil fertility due to its association with soil N supply for crop growth. Also, PMN indicates the status of soil microbial community associated with PMN, whether it is improving or degrading. Forest soils are characterized by greater levels of PMN than CT receiving conventional chemical fertilizers which could be assignable to improved microbial activity in the former soils than the latter[48,77]. Aulakh et al.[85] assessed the effect of various combinations of fertilizer N, P, FYM and wheat residue (WR) applied to soybean and soybean residues added to wheat under CT and CA. The added fertilizers of N and P, FYM, and crop residue enhanced the mean weight diameter and water-stable aggregates thus favoured the development of macro-aggregates. The treatment INF + FYM + crop residue performed better among all the treatments. The net flux of mineral nitrogen from the mineralizable fraction is used to measure potentially mineralizable N which indicates the balance between mineralization and immobilization by soil microbes[77]. Nitrogen mineralization is widely used to assess the ability of SOM to supply inorganic nitrogen in the form of nitrate which is the most common form of plant-available nitrogen. Kumar et al.[83] observed an increase in PMN which was higher in surface soil than sub-surface soil thereby implying that high OC accumulation on account of crop residue retention was the most probable cause.

    Verma & Goyal[86] assessed the effect of INM and organic manuring on PMN and observed that PMN was substantially affected by different organic amendments. Potentially mineralizable nitrogen varied between 19.6−41.5 mg kg−1 soil with greater quantity (2.5%) in vermicompost applied plots than FYM treated plots. The INF treatments resulted in lower PMN content which could be due to nutrient immobilization by microbes. Mahal et al.[87] reported that no-till resulted in higher PMN content than conventional tillage treatments. This trend was due to the maintenance of SOM due to the residue cover and reduction of soil erosion under no-tillage system[88]. On the contrary, tillage practices led to the loss of SOC owing to loosened surface soil and higher mineralization of SOM.

    Soil respiration is referred as the sum of CO2 evolution from intact soils because of the respiration by soil organisms, mycorrhizae and roots[89]. Various researchers have proposed soil respiration as a potential indicator of soil microbial activity[52,77]. Gilani & Bahmanyar[90] observed that addition of organic amendments enhanced soil respiration more than the control and synthetic fertilizer treatments. Moreover, among organic amendment treatments, highest soil respiration was observed in sewage-sludge treated soils. Under controlled conditions in saline-sodic soil, Celis et al.[91] reported that sewage sludge resulted in a higher soil respiration rate than mined gypsum and synthetic gypsum. The application of gypsum because of minimal organic matter intake had little effect on soil respiration. The addition of organic matter especially during early spring led to higher microbial biomass and soil respiration albeit diminished levels of nitrate-N. Moreover, SOM hinders the leaching of nitrate ions thereby resulting in a better soil chemical environment[71].

    Faust et al.[92] observed that microbial respiration was associated with volumetric water content. The respiration declined with less availability of water, thus the lesser the tillage intensity, the more the volumetric water content which consequently resulted in higher microbial respiration. Another study by Bongiorno et al.[93] reflected the influence of soil management intensity on soil respiration. Reduced tillage practices resulted in 51% higher basal respiration than CT. Furthermore, this investigation suggested that microbial catabolic profile could be used as a useful biological soil quality indicator. Recently, Kalkhajeh et al.[94] ascertained the impact of simultaneous addition of N fertilizer and straw-decomposing microbial inoculant (SDMI) on soil respiration. The SDMI application boosted the soil microbial respiration which accelerated the decomposition of straw due to N fertilization. The C/N ratio did not affect the microbial respiration at elongation and heading stages, whereas N fertilization enhanced the microbial respiration to a greater extent than the unfertilized control. Additionally, the interaction between sampling time and basal N application significantly affected microbial respiration.

    Gong et al.[95] apprised the effect of conventional rotary tillage and deep ploughing on soil respiration in winter wheat and observed that deep ploughing resulted in a higher soil respiration rate than conventional rotary tillage. Soil moisture content and temperature are the dominating agents influencing soil respiration which is restricted by the soil porosity.

    Soil organic carbon plays a vital role in regulating various soil functions and ecosystem services. It is influenced by numerous factors like tillage practices and fertilization. Moreover, modified management practices may prove beneficial to avoid SOC loss by increasing its content. An exogenous supply of fertilizers may alter the chemical conditions of soil and thus result in transformation of SOC. Tillage practices lead to frequent soil disturbances which reduce the size of soil aggregates and accelerate the oxidation of SOC thereby reducing its content. The literature on the influence of fertilization and tillage practices on the transformation of SOC is discussed below.

    Soil organic carbon is a major part of the global carbon cycle which is associated not only with the soil but also takes part in the C cycling through vegetation, oceans and the atmosphere (Figs 1 & 2). Soil acts as a sink of approximately 1,500 Pg of C up to 1 m depth, which is greater than its storage in the atmosphere (approximately 800 Pg C) and terrestrial vegetation (500 Pg C) combined[96]. This dynamic carbon reservoir is continuously cycling in diverse molecular forms between the different carbon pools[97]. Fertilization (both organic and mineral) is one of the crucial factors that impart a notable influence on OC accretion in the soil. Many researchers have studied the soil C dynamics under different fertilizer treatments. Though inorganic fertilizers possess the advantage of easy handling, application and storage, they do not contribute to soil organic carbon. On the contrary, regardless of management method, plant residues are known to increase organic carbon content.

    Figure 1.  Impact of different fertilization regimes on abundance of the microbial biomarker groups . Error bars represent the standard error of the means and different letters indicate significant differences at p < 0.05 among treatments. Source: Li et al.[60].
    Figure 2.  Soil organic carbon (SOC) dynamics in the global carbon cycle.

    Katkar et al.[98] reported a higher soil quality index under conjunctive nutrient management strategies comprising addition of compost and green leaves along with mineral nutrients. Mazumdar et al.[99] investigated the impact of crop residue (CR), FYM, and leguminous green manure (GM) on SOC in continuous rice-wheat cropping sequence over a 25-year period. At the surface layer, the maximum SOC content was recorded under NPK + FYM than NPK + CR and NPK + GM treatments. SOC was significantly lower under sole application of INFs (NPK) than the mixed application of organic and inorganic treatments. A higher range of SOC content was recorded at a depth of 0.6 m in the rice-wheat system (1.8–6.2 g kg−1) in farmyard manure (FYM)-treated plots than 1.7–5.3 g kg−1 under NPK, and 0.9–3.0 g kg−1 in case of unfertilized plots[100]. In a research study Dutta et al.[101] reported that rice residue had a higher decomposition rate (k¼ 0.121 and 0.076 day−1) followed by wheat (0.073 and 0.042 day−1) and maize residues (0.041 day−1) when their respective residues placed on soil surface than incorporated in the soils. Naresh et al.[102] found FYM and dhaincha as GM/ sulphitation press mud (SPM) treatments are potent enough to enhance the SOC. Maximum SOC content was noted in 0–5 cm depth that reduced gradually along the profile. In surface soil, the total organic content (TOC) under different treatments varied with source used to supply a recommended dose of nitrogen (RDN) along with conventional fertilizer (CF).

    Cai et al.[103] ascertained that long-term manure application significantly improved SOC content in different size fractions which followed the sequence: 2,000–250 μm > 250–53 μm > 53 μm fraction. Naresh et al.[22] determined that mean SOC content increased from 0.54% in control to 0.65% in RDF and 0.82% in RDF + FYM treatment and improved enzyme activity; thus, ultimately influenced nutrient dynamics under field conditions. The treatments RDF + FYM and NPK resulted in 0.28 Mg C ha−1 yr−1 and 0.13 Mg C ha−1 yr−1, respectively and thus higher sequestration than control. Zhao et al.[104] determined that in the surface layer, significant increase in SOC content in each soil aggregate was noticed under straw incorporation treatments over no straw incorporated treatments (Fig. 3). Moreover, the aggregate associated OC was significantly higher in the surface layer than the sub-surface layer. The highest increment in aggregate-associated OC was noted in both maize and wheat straw (MR-WR) added plots followed by MR and least in WR. Besides, all of the three straw-incorporated treatments exhibited notable increase in SOC stock in each aggregate fraction in the surface layer of the soil. In the subsurface (20−40 cm) layer under MR-WR, significant rise in SOC stock of small macro-aggregates was observed, whereas there was a reduction in SOC stock in the silt + clay fraction than other treatments. The straw-incorporated treatments increased the quantity of mineral-associated organic matter (mSOM) and intra-aggregate particulate organic matter, (iPOM) within small macro-aggregates and micro-aggregates especially in the topmost layer of the soil.

    Figure 3.  Distribution of OC in coarse iPOM (intra-aggregate particulate organic matter) fine iPOM, mSOM (mineral-associated matter), and free LF (free light fraction) of small macro-aggregates and micro-aggregates in the 0–20 cm and 20–40 cm soil layers under MR-WR (return of both maize and wheat straw), MR (maize straw return), WR (wheat straw return). Different lowercase and uppercase letters indicate significant differences at p < 0.05 among treatments and depths respectively[104].

    Srinivasarao et al.[105] reported that SOC content was reduced with the addition of INFs (100% RDN) alone as compared to the conjunctive application of inorganic and organic or sole FYM treatments. Earlier, Srinivasarao et al.[106] reported that FYM treated plots exhibited greater per cent increase in SOC stock than mineral fertilized plots and control. Tong et al.[107] ascertained that the application of NP and NPK significantly improved SOC stocks. On the contrary, fertilized soils could also exhibit decrease in carbon content than control. Naresh et al.[108] determined that higher biomass C input significantly resulted in greater particulate organic carbon (POC) content. Zhang et al.[109] ascertained that long-term addition of NPK and animal manures significantly improved SOC stocks by a magnitude of 32%−87% whereas NPK and wheat/ and or maize straw incorporation enhanced the C stocks by 26%−38% than control. Kamp et al.[110] determined that continuous cultivation without fertilization decreased SOC content by 14% than uncultivated soil. However, super optimum dose of NPK, balanced NPK fertilization and integration of NPK with FYM not only improved SOC content but also SOC stocks over the first year. In conventionally tilled cotton-growing soils of southern USA, Franzluebbers et al.[111] estimated that carbon sequestration averaged 0.31 ± 0.19 Mg C ha−1 yr−1. Mandal et al.[112] reported maximum SOC stock in the surface layer of the soil (0–15 cm) which progressively diminished with depth in each land use system. A significant decrease in SOC stock along the profile depth was also observed by Dhaliwal et al.[47] in both croplands and agroforestry. In the topmost soil layer, highest SOC stock was recorded in rice–fallow system while the lowest was in the guava orchard[112].

    Nath et al.[113] determined that there was accrual of higher TOC in surface layers as compared to lower layers of soil under paddy cultivation. This accrual could be adduced to left-over crop residues and remnant root biomass which exhibited a decreasing trend with soil depth. Das et al.[114] determined that integrated use of fertilizers and organic sources resulted in greater TOC as compared to control or sole fertilizer application. Fang et al.[115] observed that the cumulative carbon mineralization differed with aggregate size in top soils of broad-leaved forests (BF) and coniferous forests (CF). However, in deep soil it was greater in macro-aggregates as compared to micro-aggregates in BF but not in CF (Fig. 4). By and large, the percent SOC mineralized was greater in macro-aggregates as compared to micro-aggregates. Dhaliwal et al.[100] ascertained that SOC accrual was considerably influenced by residue levels and tillage in surface soil (0−20 cm); albeit no variation was observed at lower depth (20−40 cm). The SOC content was greater in zero-tilled and permanently raised beds incorporated with residues as compared to puddled transplanted rice and conventionally planted wheat. Pandey et al.[116] reported that no-tillage prior to sowing of rice and wheat increased soil organic carbon by 0.6 Mg C ha–1 yr–1. The carbon sequestration rate on account of no-tillage or reduced tillage ranged between 0−2,114 kg ha–1 yr–1 in the predominant cropping system of South Asia, Xue et al.[117] observed that the long-term conventional tillage, by and large, exhibited a significant decline in SOC owing to degradation of soil structure, exposing protected soil organic matter (intra-soil aggregates) to microbes. Therefore, the adoption of no-tillage could hamper the loss of SOC thereby resulting in a greater or equivalent quantity of carbon in comparison to CT (Fig. 5).

    Figure 4.  (a) Soil aggregate fractions of two depths in two restored plantations of subtropical China, (b) organic carbon and (c) its mineralization from various soil aggregates within 71 d at various soil depths in two restored plantations of subtropical China. Error bars show the standard error of the mean. The different letters represent significant differences among the different soil aggregate fractions within a depth at p < 0.05[115].
    Figure 5.  The concentrations of (a) SOC, (b) total nitrogen (TN), and (c) soil C:N ratio for 0–50 cm profile under different tillage treatments in 2012 and 2013. NT = no-till with residue retention; RT = rotary tillage with residue incorporation; PT = plow tillage with residue incorporation; and PT0 = plow tillage with residue removed. The lowercase letters indicate statistical difference among treatments at p < 0.05[117].

    Singh et al.[118] determined that carbon stock in the 0-40 cm layer increased by 39, 35 and 19% in zero-tilled clay loam, loam, and sandy loam soils, respectively as compared to conventional tilled soils over a period of 15 years. Kuhn et al.[119] also apprised about the advantages of NT over CT vis-a-vis SOC stocks across soil depths. In the surface layer (0−20 cm) NT, by and large, resulted in higher SOC stocks as compared to CT; however, SOC stocks exhibited a declining trend with soil depth, in fact, became negative at depths lower than 20 cm. Sapkota et al.[120] observed that over a period of seven years, direct dry-seeded rice proceeded by wheat cultivation with residue retention enhanced SOC at 0-60 cm depth by a magnitude of 4.7 and 3.0 t C ha−1 in zero-tillage (ZTDSR-ZTW + R) and without tillage (PBDSR-PBW + R), respectively. On the contrary, the conventional tillage rice-wheat cropping system (CTR-CTW) decreased the SOC up to 0.9 t C ha−1 (Table 2).

    Table 2.  Influence of tillage and crop establishment methods on SOC stock and its temporal variation under rice–wheat system[120].
    Tillage and crop establishment methodsDepths (m)
    0–0.050.05–0.150.15–0.30.3–0.60–0.6
    Total SOC (t/ha)
    CTR-CTW3.5e7.1c8.77.026.2c
    CTR-ZTW3.9d7.6bc8.86.526.7c
    ZTDSR-CTW4.2d7.5bc9.26.327.3c
    ZTDSR-ZTW4.9c8.9ab8.26.228.2bc
    ZTDSR-ZTW+R6.1a9.0ab9.86.831.8a
    PBDSR-PBW+R5.5b9.3a9.36.030.1ab
    MSD0.41.72.01.42.49
    Treatment effect
    (p value)
    < 0.0010.040.1580.267< 0.001
    Initial SOC content3.6 ±
    0.15
    8.1 ±
    1.39
    8.78 ±
    1.07
    6.7 ±
    0.73
    27.1 ±
    1.21
    Change in SOC over seven years (t/ha)
    CTR-CTW−0.16−0.99−0.040.28−0.90
    CTR-ZTW0.28−0.500.01−0.20−0.41
    ZTDSR-CTW0.62−0.570.45−0.340.16
    ZTDSR-ZTW1.340.84−0.62−0.461.09
    ZTDSR-ZTW+R2.490.961.040.164.66
    PBDSR-PBW+R1.891.220.51−0.642.98
    CTR-CTW = Conventionally tilled puddled transplanted rice followed by conventionally tilled wheat, CTR-ZTW = Conventionally tilled puddled transplanted rice followed by zero-tilled wheat, ZTDSR-CTW = Zero-tilled direct dry-seeded rice followed by conventionally tilled wheat, ZTDSR-ZTW = Zero-tilled direct dry-seeded rice followed by zero-tilled wheat, ZTDSR-ZTW+R = Zero-tilled direct dry-seeded rice followed by zero-tilled wheat with residue retention, PBDSR-PBW+R = Direct dry-seeded rice followed by direct drilling of wheat both on permanent beds with residue retention, MSD, minimum significant difference. Significant different letters indicate significant differences at p < 0.05.
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    Labile organic carbon (LC) is that fraction of SOC that is rapidly degraded by soil microbes, therefore, having the highest turnover rate. This fraction can turn over quickly on account of the change in land use and management strategies. From the crop production perspective, this fraction is crucial as it sustains the soil food cycle and, hence, considerably impacts nutrient cycling thereby altering soil quality and productivity. Short-term management could influence the labile fraction of carbon[121]. However, some site-specific problems and regional factors may influence their distribution in soil layers[102].

    Banger et al.[122] observed significant alteration in labile pools of C, for instance, particulate organic matter (POM), water-soluble C (WSC) and light fraction of C (LFC) because of the addition of fertilizers and/or FYM over a 16-year period. Particulate organic matter, LFC and WSC contributed 24%–35%, 12%–14% and 0.6%–0.8%, respectively, towards SOC. The increase in concentration of SOC including its pools like POC and the sequestration rate due to integrated nutrient management was also reported by Nayak et al.[123]. Gu et al.[124] observed that mulch-treated soils (straw and grass mulch) had significantly greater levels of LOC, POC, DOC and EOC as compared to no mulch-treated soils which could be adduced to the addition of straw, root and its sections into the soil. The content of labile C fractions across all treatments exhibited a decreasing trend with soil depth[23, 102, 125].

    In a long-term experiment, Anantha et al.[126] observed that the total organic carbon apportioned into labile carbon, non-labile, less labile, and very labile carbon constituted around 18.7%, 19.3%, 20.6% and 41.4% of the TOC, respectively (Table 3). Zhu et al.[20] determined that straw incorporation had a substantial impact on TOC and labile C fractions of the soil which were greater in straw incorporated treatments as compared to non-straw treatments across all the depths. Wang et al.[127] reported that the light fraction organic carbon (LFOC) and DOC were significantly greater in the straw-applied treatments than the control by a magnitude of 7%–129% for both the early and late season rice. The treatments NPK + FYM or NPK + GR + FYM resulted in greater content of very labile and labile C fractions whereas non-labile and less labile fractions were greater in control and NPK + CR treatment. There was 40.5% and 16.2% higher C build-up in sole FYM treated plots and 100% NPK + FYM, respectively over control. On the other hand, a net depletion of 1.2 and 1.8 Mg ha−1 in carbon stock was recorded under 50% NPK and control treatments, respectively. Out of the total C added through FYM, only 28.9% was stabilized as SOC, though an external supply of OM is a significant source of soil organic carbon[69]. Hence, to sustain the optimum SOC level at least an input of 2.3 Mg C ha−1 y−1 is required. A comparatively greater quantity of soil C in passive pools was observed in 100% NPK + FYM treatment. The increase in allocation of C into the passive pool was about 33%, 35%, 41% and 39% of TOC in control, suboptimal dose, optimal dose and super optimal dose of NPK which indicates that the concentration of passive pools increased with an increase in fertilization doses. Water-soluble carbon (WSC) was 5.48% greater in the upper soil layer as compared to lower layer of soil. In surface soil (0−15 cm), the values of light fraction carbon (LFC) were 81.3, 107.8, 155.2, 95.7, 128.8, 177.8 and 52.7 mg kg−1 in ZT without residue retention, ZT with 4 t ha−1 residue retention, ZT with 6 t ha−1 residue retention, FIRB without residue addition and FIRB with 4 and 6 t ha−1 residue addition and CT, respectively (Table 4). Tiwari et al.[128] determined that the decrease in POC was due to reduction in fine particulate organic matter in topsoil whereas decrement in dissolved organic carbon was observed largely in subsoil. Therefore, in surface soils fine POC and LFOC might be regarded as preliminary evidence of organic C alteration more precisely, while DOC could be considered as a useful indicator for subsoil. Reduction in allocations of fine POC, LFOC and DOC to SOC caused by tillage and straw management strategies indicated the decline in quality of SOC. A higher SOC concentration was recorded in the conjoint application of INF + FYM (0.82%) and sole application of INF (0.65%) than control (0.54%). Kumar et al.[83] reported that the CT without residue retention had significantly lower labile carbon fractions (27%–48%) than zero-tillage with 6-ton residue retention. Moreover, residue-retained fertilized treatments had significantly greater labile fractions of C than sole fertilized treatments[125]. Kumar et al.[83] reported highest change in DOC in zero-till with residue retention (28.2%) in comparison to conventional tillage practices. In ZT, absence of soil perturbations resulted in sustained supply of organic substrata for soil microbes which increases their activity. On the contrary, CT practices resulted in higher losses of C as CO2 due to frequent disturbances.

    Table 3.  Oxidisable organic carbon fractions in soils (g kg−1) at different layers[126].
    TreatmentDepths (cm)
    0−1515−3030−45Total
    Very Labile C
    Control3.6 ± 0.5c1.4 ± 0.3b1.3 ± 0.2a6.3 ± 0.4b
    50% NPK4.6 ± 0.3bc2.1 ± 0.7ab1.5 ± 0.1a8.1 ± 0.9a
    100% NPK4.4 ± 0.3bc2.3 ± 0.2a1.4 ± 0.5a8.0 ± 0.7a
    150% NPK5.0 ± 0.2ab2.6 ± 0.2a1.5 ± 0.1a9.0 ± 0.3a
    100% NPK + FYM4.8 ± 0.2ab2.0 ± 0.2ab1.3 ± 0.3a8.1 ± 0.2a
    FYM5.9 ± 1.3a2.2 ± 0.2a1.4 ± 0.3a9.5 ± 1.6a
    Fallow4.2 ± 0.7bc1.5 ± 0.5b0.7 ± 0.3b6.3 ± 0.8b
    Lbile C
    Control2.4 ± 0.3a1.0 ± 0.2a0.8 ± 0.4a4.2 ± 0.6a
    50% NPK1.7 ± 0.4ab0.9 ± 0.5a0.7 ± 0.2a3.3 ± 0.7a
    100% NPK1.8 ± 0.4ab0.8 ± 0.5a0.6 ± 0.3a3.2 ± 0.8a
    150% NPK1.2 ± 0.3b0.7 ± 0.2a0.9 ± 0.2a2.8 ± 0.4a
    100% NPK + FYM1.9 ± 0.3ab0.7 ± 0.2a0.7 ± 0.3a3.4 ± 0.2a
    FYM2.5 ± 0.9a0.7 ± 0.3a0.7 ± 0.2a3.9 ± 0.9a
    Fallow2.2 ± 1.0ab1.0 ± 0.3a1.0 ± 0.4a4.1 ± 1.1a
    Less labile C
    Control1.5 ± 0.3c0.6 ± 0.4c0.4 ± 0.0c2.6 ± 0.7d
    50% NPK1.8 ± 0.1c0.4 ± 0.1c0.5 ± 0.2c2.7 ± 0.1cd
    100% NPK2.5 ± 0.3ab0.8 ± 0.1bc1.1 ± 0.2ab4.4 ± 0.1b
    150% NPK2.6 ± 0.2a0.9 ± 0.1bc0.4 ± 0.2c3.9 ± 0.1b
    100% NPK + FYM2.7 ± 0.6a1.5 ± 0.2a1.4 ± 0.1a5.6 ± 0.7a
    FYM1.9 ± 0.7bc1.7 ± 0.2a1.0 ± 0.2b4.5 ± 0.7ab
    Fallow1.5 ± 0.3c1.3 ± 0.7ab0.9 ± 0.4b3.8 ± 1.2bc
    Non labile C
    Control1.2 ± 0.5b1.2 ± 0.3a0.2 ± 0.2b2.6 ± 0.5b
    50% NPK1.2 ± 0.9b1.7 ± 0.8a0.7 ± 0.4ab3.5 ± 1.8ab
    100% NPK1.3 ± 0.6b1.5 ± 0.6a0.5 ± 0.2ab3.3 ± 1.0ab
    150% NPK1.4 ± 0.3b1.5 ± 0.2a0.8 ± 0.1a3.7 ± 0.3ab
    100% NPK + FYM2.0 ± 0.8b1.3 ± 0.1a0.3 ± 0.3ab3.5 ± 0.7ab
    FYM3.7 ± 1.3a1.0 ± 0.2a0.5 ± 0.5ab5.1 ± 1.9a
    Fallow2.1 ± 0.2b1.4 ± 0.7a0.4 ± 0.2ab3.9 ± 0.9ab
    Values in the same column followed by different letters are significantly different at p < 0.001, ± indicates the standard deviation values of the means.
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    Table 4.  Influence of tillage and nitrogen management on distribution of carbon fractions in soil[83].
    TreatmentsWSOC
    (g kg−1)
    SOC
    (g kg−1)
    OC
    (g kg−1)
    BC
    (g kg−1)
    POC
    (mg kg)
    PON
    (mg kg−1)
    LFOC
    (mg kg−1)
    LFON
    (mg kg−1)
    Depths (cm)
    0−1515−300−1515−300−1515−300−1515−300−1515−300−1515−300−1515−300−1515−30
    Tillage practices
    ZTR28.826.223.119.39.619.134.694.281342.8967.9119.5108.1194.7154.814.812.3
    ZTWR25.324.618.414.87.877.213.763.19981.1667.494.686.5120.5104.711.810.3
    RTR27.025.922.418.28.688.174.133.871230.2836.9109.797.8170.9144.913.711.6
    RTWR23.721.818.114.27.667.073.122.96869.4604.482.676.6107.197.39.78.6
    CTR26.124.421.817.48.497.963.823.481099.1779.498.489.3143.8115.912.810.9
    CT21.820.916.113.16.215.642.892.63617.5481.869.257.690.873.69.67.9
    Nitrogen management
    Control21.114.916.113.16.135.481.581.07709.7658.631.726.3123.9104.36.45.8
    80 kg N ha−128.321.217.814.76.466.162.461.75860.7785.668.456.2132.8116.17.66.9
    120 kg N ha−129.522.119.116.17.256.713.262.18952.2808.989.578.5150.6127.69.78.6
    160 kg N ha−130.223.120.818.27.757.283.822.661099.5823.896.883.4168.5145.710.29.8
    200 kg N ha−131.125.421.318.77.937.484.153.421153.1898.4103.997.3176.2152.911.710.6
    WSOC = Water soluble organic carbon, SOC = Total soil organic carbon, OC = Oxidizable organic carbon, BC =Black carbon, POC = particulate organic carbon, PON = particulate organic nitrogen, LFOC = labile fraction organic carbon, and LFON = labile fraction organic nitrogen. ZTR = Zero tillage with residue retention, ZTWR = Zero tillage without residue retention; RTR = Reduced tillage with residue retention, RTWR = Reduced tillage without residue retention, CTR = Conventional tillage with residue incorporation; CT = Conventional tillage without residue incorporation.
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    The soil characteristics such as plant available nutrients, microbial diversity and soil organic carbon transformation are dwindling on account of intensive cultivation under conventional tillage practices, therefore, demand relevant management approaches for soil and crop sustainability. Long-term application of organic amendments significantly increases soil properties by increasing plant available macro, micro, secondary nutrients and soil organic C, whereas the increase in organic C by INF application is, by and large, due to increment in organic C content within macro-aggregates and in the silt + clay compartments. The soil organic carbon and other plant available nutrients were significantly greater in conservation tillage systems as compared to conventional tillage (CT) that conservation approaches could be an exemplary promoter of soil productivity by modifying soil structure thereby protecting SOM and maintaining higher nutrient content. The mean concentration of different fractions of carbon MBN, PMN and soil respiration under integrated nutrient management treatments was higher as compared with to control. Therefore, the conjoint use of organic manures or retention of crop residues with inorganic fertilizers is imperative to reduce the depletion of SOC while sustaining crop production as a realistic alternative. Future research should focus mainly on the usage of organic and mineral fertilizers in conjunction with conservation tillage approaches to sustain the soil environment.

    The authors confirm contribution to the paper as follows: study conception and design: Dhaliwal SS, Shukla AK, Randhawa MK, Behera SK; data collection: Sanddep S, Dhaliwal SS, Behera SK; analysis and interpretation of results: Dhaliwal SS, Gagandeep Kaur, Behera SK; draft manuscript preparation: Dhaliwal SS, walia, Shukla AK, Toor AS, Behera SK, Randhawa MK. All authors reviewed the results and approved the final version of the manuscript.

    Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

    The support rendered by the Departemnt of Soil Science, PAU, Ludhiana, RVSKVV, Gwailor, CSSRI, Karnal, IISS, Bhopal, School of Organic Farming, PAU Ludhiana and Washington State University, USA is fully acknowledged .

  • The authors declare that they have no conflict of interest.

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  • Cite this article

    Zou Y, Wang X, Li L, Wang L, Lan Y, et al. 2023. Preparation, structure and antimicrobial properties of modified gelatin composite hydrogel from chicken, bovine and porcine lung. Food Materials Research 3:35 doi: 10.48130/fmr-0023-0035
    Zou Y, Wang X, Li L, Wang L, Lan Y, et al. 2023. Preparation, structure and antimicrobial properties of modified gelatin composite hydrogel from chicken, bovine and porcine lung. Food Materials Research 3:35 doi: 10.48130/fmr-0023-0035

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ARTICLE   Open Access    

Preparation, structure and antimicrobial properties of modified gelatin composite hydrogel from chicken, bovine and porcine lung

Food Materials Research  3 Article number: 35  (2023)  |  Cite this article

Abstract: In this paper, the reaction process parameters of the hydrogel produced by the modified gelatin from chicken, bovine and porcine lungs with carboxymethyl chitosan (CMCS) and oxidized glucomannan (OKGM) were optimized to produce Schiff base reaction. The results showed the properties of the three composite hydrogels are improved when the value of gelatin/CMCS/OKGM reached 1:2:2. The best modified gelatin/CMCS/OKGM of bovine lung composite hydrogel (COBH) had a gelatin strength of 8.14 N, a swelling rate of 257%, a water evaporation rate of 66.86%, and an antibacterial property of 38.02%. The properties of modified gelatin/CMCS/OKGM of chicken lung composite hydrogel (COCH) were similar to those of COBH. However, the water holding capacity of COCH was higher than that of COBH. The properties of the modified gelatin/CMCS/OKGM for porcine lung composite hydrogel (COPH) were significantly decreased over those of the other two. Therefore, COCH has potential applications in food coating and preservation.

    • In recent years, hydrogels, as an important new class of biomaterials, can be used by oxygen, drug molecules and other water-soluble small molecules through. Therefore, it is widely used in the fields of tissue engineering[1], drug delivery[2], edible films[3] and biosorbents[4]. Gelatin is homologous with collagen, it has good thermal reversibility, water binding ability, film forming, foaming and emulsifying ability. Gelatin can be converted to hydrogel by using physical, chemical and enzymatic treatments[5]. The search for alternative sources of bovine and porcine gelatin has been put on the agenda due to bovine spongiform encephalopathy and Islamic religious beliefs. Aquatic products also contain abundant collagen, but their thermal stability is worse than that of terrestrial organisms. Chicken lung contains a large amount of collagen, with a content of 3.0%−3.5%, which can be used for the extraction of gelatin. The annual slaughter volume of broilers is as high as 100 billion in China. Chicken lungs, as by-products of their processing, were mostly treated as waste. They were not only polluted the environment but also wasted resources. Through preliminary study by our team, it was found that chicken lungs were rich in collagen.

      Carboxymethyl chitosan (CMCS), as a chitosan derivative, has physical and biological properties such as gelling, film-forming, antibacterial and good biocompatibility[6]. Cao et al.[7] prepared a CMCS/oxidized carboxymethylcellulose/curcumin film using the cast film method, which showed good color protection and mold growth inhibition for freshness preservation as a coated antibacterial material. Polysaccharide hydrogels have many advantages, but also disadvantages such as poor mechanical properties and unstable gelatin performance have limited their practical application in industrial production.

      Konjac glucomannan (KGM) has good biocompatibility, high viscosity and is biodegradable[8] as well as regulating intestinal function, lipid metabolism[9] and other functions. During the oxidation reaction, aldehyde groups are generated in the KGM molecular chains, which are chemically cross-linked by the Schiff base reaction between the free amino group of CMCS and the aldehyde group of OKGM, enhancing the mechanical properties and functionality of the hydrogel[6]. In this paper, hybrid hydrogels were made by cross-linking lung-modified gelatin with CMCS and OKGM, and the structure and properties of the hydrogel composite system were analyzed. The effect of different OKGM mixing ratio on hydrogel performance was studied to find composite hydrogels with good performance.

    • Modified gelatin of chicken, bovine and porcine lung was homemade in the laboratory, whose content of collagen was 20% and 30%, respectively. Briefly, lung gelatin is dissolved in phosphate solution followed by the addition of ethylenediamine and 1-Ethyl-3-(3-dimethylaminopropyl) carbodimide hydrochloride (EDC). The modified lung gelatin was obtained after heating at 37 °C for 2 h and filtering through a 3,500 kDa dialysis bag for 3 d. Carboxymethyl chitosan, konjac glucomannan, sodium periodate, and ethylene glycol were purchased from Shanghai Maclean Biochemical Technology Co., Ltd. (Shanghai, China). Brain heart infusion broth ulture medium was purchased from Qingdao Haibo Biotechnology Co., Ltd. (Qingdao, China). The remaining substances were all analytical-grade compounds and solvents.

    • The experimental method of OKGM preparation was using the method of Jiang et al.[10] with slight modification. KGM (5 g) was put into a 250 mL beaker. Deionized water (150 mL) was added and they were mixed well. They were divided into seven groups and 10 mL of 0.04, 0.06, 0.08, 0.10, 0.12, 0.14, and 0.16 g/mL of NaIO4 solution was added dropwise, respectively. After measuring the optimal oxidant concentration conditions, the mixture was stirred in the dark, at room temperature for 8, 9, 10, 11, 12, 13, and 14 h, respectively. An equimolar amount of ethylene glycol with NaIO4 was added and stirred for 2 h to terminate the reaction. The mixture was dialyzed with 3,500 kDa dialysis bag for 3 d until the solution was free of periodate (checked with silver nitrate). The dialysates were frozen and lyophilized in a freeze-dryer for subsequent measurements.

    • The determination of aldehyde group content for OKGM was carried out according to the method of Yan et al.[11] with slight modification. OKGM (0.2 g) was dissolved in 50 mL of hydroxylamine-methyl orange hydrochloride solution and mixed well for 2 h. The samples were titrated with 0.1 mol/L NaOH standard solution and stopped when the color of the solution was changed from orange-red to light yellow with the last pH of 5.0. The titration curve was plotted using the volume of NaOH standard liquid consumed as the horizontal coordinate and the pH value as the vertical coordinate.

      Aldehydegroupconcentration=ΔV×0.001×nNaOHW

      Where: ΔVis the volume of NaOH standard liquid consumed at the end of the titration. nNaOH is the molar concentration of NaOH standard solution. W is the mass of OKGM.

    • In this experiment, CMCS (4%, w/v), OKGM (4%, w/v) and modified lung gelatin (15%, w/v) were used to prepare hydrogel by our previous study. The volume ratio of CMCS: aminized lung gelatin: OKGM solution was homogeneously mixed of 1:2:1, 1:2:2, 1:2:3, 1:2:4. Three of the above different mixture of chicken, bovine and porcine lung modified gelatin/CMCS/OKGM composite hydrogels, named COCH-1, COCH-2, COCH-3, COCH-4, COBH-1, COBH-2, COBH-3, COBH-4, COPH-1, COPH-2, COPH-3, and COPH-4, respectively, were prepared.

    • FTIR spectroscopy was determined using the method described by Shi et al.[12]. The FTIR spectra of samples were analyzed with a 32 scans/min at a resolution of 4 cm−1 in 400 cm−1 and 4,000 cm−1.

    • The determination of scanning electron microscope (SEM) characterization was carried out as using the method of Shi et al.[12] with slight modification. The microstructure of the upper surface of the samples was visualized using a scanning electron microscope at an accelerating voltage of 10 kV. Prior to visualize, the samples were mounted on a brass stub and sputtered with gold in order to make the sample conductive, and photographs were taken at 8000× magnification for surface.

    • Gelatin strength was determined using the method described by Fan et al.[13]. The texture instrument was set to TPA gel strength mode. The Bloom gel strength was determined with the texture analyser, which was set to a P36R probe with a starting force of 0.15 N and a speed of 2 mm/s to 80% deformation.

    • The experimental method of swelling rate of samples was carried out using the methods of Fan et al.[14] with slight modification. The hydrogels were freeze-dried into uniformly sized discs and the weight was recorded as M0. The hydrogel was dissolved in PBS buffer of pH 7.4 at 37 °C, which was weighed again after every interval and recorded as M1.

      SwellingrateESR(%)=m1m0m0×100%
    • The experimental method of thermal variation analysis was carried out using the methods of Bai et al.[4] with slight modification. The sample was placed in a thermogravimetric analyzer for thermal stability analysis. Dried samples (0.2 g) were scanned using a thermogravimetric analyser from 20 to 400 °C at a rate of 10 °C/min. Nitrogen was used as the purge gas at a flow rate of 60 mL/min.

    • The method of Liu et al.[15] was used to determinate moisture evaporation rate of the samples. The hydrogel was freeze-dried into uniform-sized discs. The hydrogel was immersed in distilled water and then left until it reached dissolution equilibrium. The water on the surface of the hydrogel was wiped away by absorbent paper and the weight was recorded as m1. The hydrogel was then placed in a constant temperature oven and weighed periodically until constant.

      Moistureevaporationrate=m1m2m1m3×100%

      where m1, m2, m3 are the initial weight, measured weight and final weight of the hydrogel, respectively.

    • LF-NMR was calculated following the procedure outlined by Jiang[16]. An instrument was used to obtain relaxation curves of the hydrogel at 25.0 °C. Sixteen scans (acquisitions) were accumulated to increase the signal-to-noise ratio. The recycle delay between the scans was 10 s to allow full spin relaxation. The pulse spacing was set to 0.4 ms between 90° and 180° pulses and the number of echoes was 15,000. Each sample was measured twice.

    • The method of Bian et al.[17] was used to measure antimicrobial properties of samples. The inhibition of COCH, COBH and COPH hydrogels on Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli) was determined by spectrophotometry. The pH of the brain heart infusion medium was adjusted to 7.2 with NaOH solution, and then sterilized in an autoclave for 15 min. The prepared hydrogels were irradiated by UV for 1 h before the experiment, and the medium without hydrogels was used as a blank control. Three equal weights of hydrogels were added to the medium and mixed well and then 200 μL of diluted bacterial solution was inoculated into the medium. The absorbance values were measured at 600 nm after the samples were continuously oscillated at 37 °C and 120 r/min for 12 h.

      Bacteriainhibitionrate=A0A1A0×100%

      Where, A1 is the absorbance after adding these composite hydrogels, and A0 is the absorbance of the control group.

    • Means ± standard deviations were used to represent the data. SPSS 19.0 program, a one-way analysis of variance (ANOVA) and Duncan's test were performed to evaluate the differences between the data.

    • The principle of oxidative modification for OKGM is to use oxidants to oxidize the hydroxyl groups on polysaccharides into carboxyl and aldehyde groups. The effect of aldehyde group content in OKGM after oxidation was explored by different oxidation times when oxidation temperature and NaIO4 concentration were constant. As shown in Fig. 1a, the content of aldehyde group of OKGM was increased with the increase of oxidation time before 12 h. A maximum value of 7.96 mmol/g of aldehyde group content was occurred at 12 h of oxidation, which was used to oxidize OKGM.

      Figure 1. 

      Aldehyde content of OKGM prepared under different (a) oxidation times and (b) oxidant concentrations. The data in this figure is expressed as mean ± SD, different letters in this curve indicate significant differences (p < 0.05).

      The effect of different NaIO4 concentrations on the content of aldehyde groups was investigated in oxidized OKGM at constant oxidation temperature and time. The results are shown in Fig. 1b. The aldehyde content in OKGM was gradually increased with the increase of NaIO4 concentration. Due to the increase of NaIO4 concentration, the cleavage of C=C of KGM into aldehyde groups was intensified, and the content of aldehyde groups was significantly increased. When the concentration of NaIO4 was higher than 0.12 g/mL, the aldehyde content of OKGM was decreased with the increase of oxidant concentration. It was due to that, the aldehyde group on the chain of OKGM molecule might be combined with the unoxidized residual hydroxyl group to form a hemiacetal structure with the increase of NaIO4 concentration. Therefore, the oxidation condition of OKGM was obtained by 0.12 g/mL NaIO4 for 12 h to prepare hydrogel.

    • The infrared spectra of COCH, COBH and COPH in the range of 4,000−500 cm−1 are shown in Fig. 2. It can be seen that the three composite hydrogels COCH-1, COBH-1 and COPH-1 had the absorption peaks at 3,400, 1,638, 1,576, and 1,236 cm−1. The wave number of 3,400 cm−1, which were corresponded to the stretching vibrations of -OH and -NH2. The absorption amide I band was corresponded to 1,638 cm−1. The bending vibration peak of -NH2 was at 1,576 cm−1. The absorption peak of the symmetric stretching vibration of -COO- was at 1,416 cm−1, and the absorption band of –OH was at 1,236 cm−1[18].

      Figure 2. 

      Infrared spectra of (a) COCH, (b) COBH and (c) COPH with different mixing ratios.

      When the ratio of OKGM increased, the spectrogram of COCH-2, COCH-3, COCH-4, COBH-2, COBH-3, COBH-4, COPH-2, COPH-3, and COPH-4 produced new vibrational stretching peaks of C=N bonds (1,638 cm−1). This appearance indicated that the aldehyde group in the OKGM molecule was cross-linked with the amino group in the CMCS or lung gelatin molecule to form a composite hydrogel. This phenomenon was also found in the infrared spectra of carboxybutyryl chitosan-serine peptide/OKGM injectable hydrogels by Wang et al.[19] Additionally, when the proportion of OKGM was increased, the corresponding absorption peaks at 1,576 cm−1 and 1,236 cm−1 were weakened. It showed that the aldehyde group and the amino group had been condensed. The Schiff base reaction had been occurred, and the composite hydrogel had been successfully cross-linked. The broad absorption band of the three composite hydrogels at 3,300 cm−1 was the absorption peak of the stretching vibration of the O-H group and the N-H group. The absorption peak was become wider when the increase of the proportion of OKGM addition. It was possible that the -OH in KGM was interacted with the -NH2 in CMCS to form a hydrogen bond. Therefore, a broader absorption peak appeared[20]. This phenomenon was consistent with the result of composite packaging films prepared by Tian et al.[21] The results showed that the three preparations had good compatibility and can be used as active ingredients to improve the composite hydrogels.

    • The role of porosity and interconnectivity in hydrogels is important for resistance to bacterial proliferation and water retention functions[22]. Figure 3 shows the internal microscopic morphology of various hydrogels at 20 μm. It was clear that all the composite hydrogels prepared by adding different proportions of OKGM had similar porous structures. The pores inside the hydrogel were interconnected and varied in size from 5−150 μm. The pore size of the composite hydrogel with a high percentage of OKGM was smaller than that of the composite hydrogel with a low percentage of OKGM. It was caused by the cross-linking between OKGM and CMCS, and the two had good compatibility and miscibility[23]. The crosslinking degree of the hydrogel was increased, the pore size was gradually reduced, and the pores were dense. More three-dimensional network structures were formed in the composite hydrogel. Similar conclusions were also obtained by Wu et al.[24]. When the OKGM ratio was increased, there were entangled clusters in SEM. It may be that the molecular weight of OKGM was large and some unreacted OKGM molecular chains were folded and bound to form tangled clusters. According to the microstructure, the porous internal structure within the composite hydrogel could be applied to drug encapsulation and slow release as well as cell culture utilization, etc.

      Figure 3. 

      Microstructure of COCH, COBH and COPH with different mixing ratios.

    • The mechanical properties of COCH, COBH, and COPH are depicted in Fig. 4. As shown in Fig. 4, among the four hydrogels with the same configuration ratio, COBH had the highest gelatin strength, followed by COCH. However, COPH hydrogel had the lowest gelatin strength. According to the ratio of OKGM addition, the highest gelatin strength of hydrogel was obtained when the ratio of OKGM addition was 1:2:2. The lowest gelatin strength of hydrogel was obtained by the ratio of 1:2:4. The gelatin strength of the composite hydrogels in COCH, COBH, and COPH with a mixing ratio of 1:2:2 was significantly increased. The gelatin strength of the gelatin-chitosan-sodium alginate composite gelatin was 5.95 N as reported by Liu et al.[25]. The gelatin strength of the hydrogel made in this study was increased four times, compared with the chitosan/bletin gum hydrogel (202.40 ± 6.35 g) prepared by Luo et al.[26]. These results indicated that the gelatin strength of the hydrogels was increased to some extent with the increase of OKGM content, which showed a positive correlation with the study of Xiong[27]. He found that the strength, hardness and adhesion of the composite hydrogel was increased with the increase of polysaccharide. This may be due to the cross-linking of the hydrogel being deepened, leading to an increase in gelatin strength. Schiff base reaction was produced continuously when the ratio of OKGM increased. But the gelatin strength of hydrogel was reduced when OKGM was added with an excessive proportion. It was possible that the hybrid hydrogel might be over-crosslinked to exhibit excessively brittle mechanical properties when the aldehyde group content was too high[28]. Three composite hydrogels of the same mixing ratio were exhibited with different gelatin strengths probably due to their different species origin. Hydrogels usually prepared from high molecular weight gelatin were shown to have high gelatin strength[29].

      Figure 4. 

      Gelatin strength of COCH, COBH and COPH with different mixing ratios. The data in this figure is expressed as mean ± SD, different letters in the same material indicates significant differences (p < 0.05).

    • In general, a good food adhesive or coating film can be characterized by the swelling ratio of the hydrogel to its ability to absorb and retain water. As the lyophilized hydrogel was soaked for a longer time, the overall trend of the composite hydrogel swelling was to first increase rapidly and then level off. The results showed that the composite hydrogel had better water absorption and water retention capacity. Composite hydrogels swelled because of hydrophilic groups such as hydroxyl, amino and amide groups in their structure, which allowed the hydrogel to hold a large number of water molecules[30]. As shown in Fig. 5, the swelling rate of composite hydrogels with mixing ratios of 1:2:2, 1:2:1, 1:2:3, and 1:2:4 was gradually decreased, respectively. In general, the high concentration of OKGM was caused the dissolution rate of the composite hydrogel to be reduced. These results were to be expected. This result indicated that increasing the concentration of OKGM allowed the degree of cross-linking to be increased, the pore size to be reduced (as shown in Fig. 5), and the swelling ratio to be reduced[31]. It can be seen that the swelling rate of hydrogel reached the highest level when the mixing ratio of OKGM was 1:2:2. The lowest swelling of the composite hydrogel with a mixing ratio of 1:2:4 might be due to the tightness of its internal structural cross-linked network, which made it difficult for water molecules to enter, and the internal water was firmly locked in the gelatin network. The COBH with the highest swelling ratio had a higher maximum swelling ratio compared to the OKGM/CMCS/graphene oxide hydrogel made by Fan et al.[6] for use as a wound dressing.

      Figure 5. 

      Swelling rate of (a) COCH, (b) COBH, and (c) COPH with different mixing ratios.

    • The thermal stability of various composite hydrogels can be studied by DSC analysis and the results are shown in Fig. 6. The three composite hydrogels had an absorption peak at 60−75 °C at a mixing ratio of 1:2:1. When the mixing ratio of OKGM was increased, the previous absorption peak was disappeared. This result indicated that Schiff base reaction occurs cross-linking was produced (as shown in Fig. 2). The complex and stable network structure was constructed by covalent and non-covalent bonding of polysaccharides and proteins, which increased the denaturation temperature.

      Figure 6. 

      Thermogravimetric analysis of (a) COCH, (b) COBH, and (c) COPH with different mixing ratios.

      As can be seen from Fig. 6, the thermal variation curves of all hydrogel samples showed similar trends. When the temperature ranges from 0 to 120 °C, the reduction of the initial mass of the sample was mainly due to the evaporation of water.[32] Subsequently, mass loss can be attributed to the degradation of exposed OKGM, CMCS and lung-modified gelatin side chains. Polysaccharides were decomposed at high temperatures to produce gaseous products and solid coke.[33] A central peak region appeared near 230 °C. The main reason might be due to the cleavage of physical forces such as electrostatic forces, hydrogen bonds and van der Waals forces in the internal structure of the hydrogel and the imine bonds in the Schiff base reaction. The phenomenon was the same as the results of the collagen-hyaluronic acid in situ hydrogel thermal transformation study trend studied by Ying[34]. Further cross-linking of hydrogels led to an increase in thermal denaturation temperature. In this study, the peak areas of the hydrogels prepared with three different mixing ratios and the positions of the peak temperatures corresponding to the regions of the reaction peaks were showed slight deviations. This result suggested that the different strength of interactions within these hydrogels might be related to their different access sources.

    • In general, the moisture content of a food product is very closely related to its food quality. Therefore, the edible and nutritional qualities of foods with lower water evaporation rates can be better preserved. Figure 7 showed the water evaporation rate of hydrogels with different mixing ratios. It can be seen that the water loss rate of all hydrogels was increased rapidly in the first 12 h and then reached a constant percentage in 24 h and maintained 20% to 25% of water content. The results showed that these composite hydrogels all had a low water evaporation rate. The final water evaporation rates of the three composite hydrogels with 1:2:4 mixing ratios in this study were better than the OKGM/CMCS/graphene oxide hydrogels made by Fan et al.[6] The water loss rate of hydrogel was gradually reduced when the OKGM content gradually increases. This might be due to the gradual stabilization of the structure of the gelatin network and the weakening of water mobility within the gelatin structure, as can be seen in Figs 3 & 5. Additionally, the water evaporation rate of three composite hydrogels with the same mixing ratio was the best for COBH and the worst for COPH. It might be related to its gelatin type, and the water holding capacity was affected by the different content of hydrophobic groups in gelatin[35]. This result also affected the water evaporation rate of the composite hydrogel produced.

      Figure 7. 

      Moisture evaporation rate of (a) COCH, (b) COBH, and (c) COPH with different mixing ratios.

    • The distribution and state of moisture in meat used LF-NMR techniques to analyze the relaxation properties of hydrogen nuclei in samples by measuring them in a magnetic field[36]. The differences in relaxation times and signal magnitudes of T2 inversion spectra were used to analyze the moisture distribution and migration patterns of COCH, COBH and COPH. As shown in Table 1, the T2 relaxation inversion spectrum varied from 0.01 to 10,000 ms, and recorded as T21 (0.01−10 ms), T22 (10−100 ms), and T23 (100−1,000 ms) in that order. These three corresponded to bounding water, non-fluidizable water and free water in the composite hydrogel[37]. Binding water (T21) value was the smallest, which was mainly in cell wall fibrous structures, polysaccharide structures, and sieve tube and duct pores[38]. Non-fluidizable water (T22) value was the next best, which was mainly in the cytoplasm in the form of enzymes, hydrated hemisaccharides, intermediate metabolites, and macromolecules. The free water (T23) value was the largest and it existed mainly in free form in the vesicles. Additionally, the T2 peak area in the spectrum was proportional to the number of hydrogen protons in the sample[39]. Therefore, the content of water in the three states of bounding water, non-fluidizable water and free water were represented by P21, P22 and P23.

      Table 1.  Low-field nuclear magnetic characterization of COCH, COBH and COPH with different mixing ratios.

      T21 (ms)T22 (ms)T23 (ms)P21P22P23
      COCH-13.152 ± 0.437a27.466 ± 0.953a530.627 ± 0.100e24.990 ± 0.394d7649.545 ± 0.963m173.803 ± 3.172d
      COCH-22.676 ± 0.487a19.902 ± 0.468c526.32 ± 0.798e27.593 ± 0.585c,d7914.01 ± 1.024h166.833 ± 2.574e
      COCH-31.978 ± 0.633a,b17.544 ± 0.200c,d581.293 ± 1.175d30.025 ± 0.370c7972.7 ± 1.590e167.659 ± 0.626e
      COCH-40.675 ± 0.088c14.759 ± 0.058d332.846 ± 0.881h32.866 ± 0.355a,b8506.39 ± 3.585b153.705 ± 1.037g
      COCH-12.7845 ± 0.731a23.558 ± 1.133b581.118 ± 1.000d35.838 ± 1.079a7775.183 ± 2.558l178.562 ± 1.297d
      COCH-22.401 ± 1.091a17.012 ± 1.604c,d483.093 ± 1.696g30.917 ± 0.319c7944.58 ± 3.422g161.966 ± 0.922f
      COCH-31.5705 ± 0.484a,b17.6185 ± 1.017c,d504.607 ± 0.050f33.752 ± 1.111a8295.7 ± 0.714d153.496 ± 2.485g
      COCH-40.557 ± 0.086c13.601 ± 0.200d303.613 ± 0.945i33.392 ± 0.177a8912.46 ± 2.481a124.857 ± 0.607h
      COPH-13.382 ± 0.260a26.308 ± 0.714a719.183 ± 1.966b26.274 ± 3.302c,d7403.543 ± 0.526n256.824 ± 0.806a
      COPH-22.675 ± 1.422a19.635 ± 0.999c627.106 ± 0.112c28.1985 ± 0.773c,d7857.69 ± 1.734i216.393 ± 0.314b
      COPH-32.072 ± 1.050a17.586 ± 0.048c,d765.049 ± 1.832a31.524 ± 0.061b7952.09 ± 1.003f193.956 ± 1.258c
      COPH-41.548 ± 0.108b16.209 ± 1.508c,d506.198 ± 1.641f31.542 ± 0.182b8331.59 ± 0.7845c176.078 ± 2.867d
      The data in this table is expressed as mean ± SD, different letters in the same column indicates significant differences (p < 0.05).

      As shown in Table 1, with the constant addition ratio of CMCS and modified gelatin, P21 and P22 of COCH, COBH and COPH showed an increasing trend and P23 showed a decreasing trend with the increasing addition of OKGM. This indicated that the conversion of free water to non-fluidizable water and bounding water in the hydrogel was gradually enhanced as the ratio of OKGM increased, resulting in an increase in water retention capacity. This reason might be due to the generation of Schiff base reaction. The internal network structure of hydrogel became more dense. The free water was converted into non-fluidizable water, and the stability was greatly enhanced. Additionally, the value of homogeneous hydrogel T23 gradually decreased with the increase of OKGM addition. This result was similar to the previous study by Chitrakar et al.[40], who suggested that the mobility of water was decreased with the addition of polysaccharides due to the binding between polysaccharide molecules. As the concentration of polysaccharides increased, tighter linkages between polysaccharide molecules occurred, depending mainly on the molar mass of the polysaccharide and inter-chain interactions[41]. At the same time, water molecules were slower to reorient in denser network structures because they were more tightly bound to biopolymers with hydrogen bonds[42]. The decrease in T23 value was due to that more water molecules were locked in the polysaccharide structure resulting in a gradual decrease in mobility as the polysaccharide concentration increases.

    • Hydrogels with antibacterial properties have a wide range of potential applications in the food industry. Figure 8 represents the inhibition of E. coli and S. aureus by composite hydrogels at different mixing ratios. The results showed that all composite hydrogels exhibited inhibitory effects on both E. coli and S. aureus. The best antibacterial effect of composite hydrogel was COBH hydrogel. When the hydrogel mixing ratio was 1:2:2, the antibacterial effect of E.coli was 38.02%, and the antibacterial effect of S.aureus was 37.39%. Because more CMCS can cross-link with OKGM to form a hydrogel with a network structure and thus the antibacterial activity was enhanced when the OKGM content increased. This result was consistent with the finding of Bozaci et al.[43] When the CMCS content in hydrogel films was 6%, the corresponding films exhibited desirable antimicrobial properties. CMCS had an inhibitory effect on bacteria by changing the permeability of the bacterial cell wall through the interaction of its cations with the anionic groups of the bacterial cell wall.[44] However, as the OKGM content continued to increase, the antibacterial activity of the hydrogel was slightly weakened instead of enhanced. This appearance was due to the fact that the gelatin structure became denser in structure, the pore size became smaller, and the carboxymethyl group was difficult to contact with bacteria. These composite hydrogels of COBH and COCH can be used in food packaging and preservation.

      Figure 8. 

      (a) Anti-S. aureus and (b) E. coli activity of COCH, COBH and COPH with different mixing ratios.

    • In this paper, the swelling rate, gelatin strength, and antibacterial properties of composite hydrogel increased initially and then decreased with the increase of OKGM ratio. The best swelling performance, gel strength and the strongest inhibition of E. coli and S. aureus was observed when lung gelatin/CMCS/OKGM was added in the ratio of 1:2:2 for COCH, COBH and COPH, respectively. The water evaporation rate of composite hydrogels all gradually decreased with the increase of OKGM ratio. The lowest water evaporation rate was achieved when the lung gelatin/CMCS/OKM addition ratio was 1:2:4. Interestingly, the hydrogel properties of COCH and COBH were interchangeable, but all were significantly different from COPH. Therefore, COCH have potential applications in food coating and preservation.

    • The authors confirm contribution to the paper as follows: methodology: Zou Y, Lan Y, Qin X, and Wang Z; validation & formal analysis : Zou Y; resources: Wang D; investigation: Zou Y, Wang X, Liang Li, Wang L, Lan Y, Qin X, Wang Z, and Wang D; draf manuscript: Zou Y, Wang X, Liang Li, and Wang L; review & editing manuscript: Wang X, Liang Li, and Wang L; project administration: Xu W. All authors reviewed the results and approved the final version of the manuscript.

    • All data generated or analyzed during this study are included in this published article.

      • This work was supported by the China Agriculture Research System (CARS-41) and Key Research, Jiangsu Agriculture Science and Technology Innovation Fund (CX (21)2016) and Liaocheng Science and Technology Support SME Climbing Plan Project (2023PDJH23).

      • The authors declare that they have no conflict of interest.

      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press on behalf of Nanjing Agricultural University. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (8)  Table (1) References (44)
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    Zou Y, Wang X, Li L, Wang L, Lan Y, et al. 2023. Preparation, structure and antimicrobial properties of modified gelatin composite hydrogel from chicken, bovine and porcine lung. Food Materials Research 3:35 doi: 10.48130/fmr-0023-0035
    Zou Y, Wang X, Li L, Wang L, Lan Y, et al. 2023. Preparation, structure and antimicrobial properties of modified gelatin composite hydrogel from chicken, bovine and porcine lung. Food Materials Research 3:35 doi: 10.48130/fmr-0023-0035

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