Carbon accumulation efficiency of granulated straw incorporation and its response to nutrient supplement in infertile agricultural soils: Evidence from biomarkers

Highlights

	● Granulated straw (GS) incorporation rapidly promoted soil carbon (C) over 80% than control.
	● The efficiency of straw-C converted into soil organic C pool was ~50% in soils.
	● GS and nutrient (GSN) incorporation reduced soil C by 11.3% in upland than GS.
	● GSN incorporation enhanced soil C by 2.2% than GS in paddy via microbial necromass.

Abstract

Granulating fluffy straw into high-density particles is an innovative approach for uniformly incorporating straw into plough layers. However, massive granulated straw incorporation probably causes microbial nutrient limitation, decreasing straw-C accrual and crop yield. Whether nutrient supplement increases straw-C accumulation remains unclear. In this study, we conducted one-year of micro-plot experiments incorporating massive granulated straw with initial C:N ratio (GS) and adjusted the C:N ratio by nutrient supplement (GS_N) in infertile upland and paddy. After one year,GS incorporation greatly improved the surface (0–20 cm layer) soil organic C by 91% and 80% in upland and paddy, respectively, compared to their control. In upland, GS led to lower lignin phenols but higher amino sugars than paddy owing to its stronger microbial anabolism. In upland, GS_N incorporation decreased soil organic C by 11.3% than GS by reducing lignin phenols and amino sugars. However, GS_N incorporation increased organic C by 2.2% in paddy, via promoting microbial necromass accumulation. GS_N incorporation improved crop yield by 26.6% in upland and 12.0% in paddy than GS. Collectively, granulated straw incorporation effectively enhances organic C and crop yield but that responses to nutrient supplement depend on soil properties. Tailored nutrient management is crucial to optimizing C sequestration and productivity in diverse soils.

Graphical abstract

Keywords

granulated straw incorporation / nutrient supplement / infertile agricultural soil / plant-derived C / microbial-derived C / microbial C metabolism

References

[1] Atere, C.T., Gunina, A., Zhu, Z.K., Xiao, M.L., Liu, S.L., Kuzyakov, Y., Chen, L., Deng, Y.W., Wu, J.S., Ge, T.D., 2020. Organic matter stabilization in aggregates and density fractions in paddy soil depending on long-term fertilization: tracing of pathways by ¹³C natural abundance. Soil Biology and Biochemistry149, 107931.

[2] Averill, C., Waring, B., 2018. Nitrogen limitation of decomposition and decay: how can it occur?. Global Change Biology24, 1417–1427.

[3] Bååth, E., Anderson, T.H., 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology and Biochemistry35, 955–963.

[4] Bahri, H., Dignac, M.F., Rumpel, C., Rasse, D.P., Chenu, C., Mariotti, A., 2006. Lignin turnover kinetics in an agricultural soil is monomer specific. Soil Biology and Biochemistry38, 1977–1988.

[5] Bossio, D.A., Scow, K.M., 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology35, 265–278.

[6] Burgess, M.S., Mehuys, G.R., Madramootoo, C.A., 2002. Decomposition of grain-corn residues (Zea mays L. ): a litterbag study under three tillage systems. Canadian Journal of Soil Science82, 127–138.

[7] Cai, Z.C., 1996. Effect of land use on organic carbon storage in soils in eastern China. Water, Air, and Soil Pollution91, 383–393.

[8] Chen, J., Seven, J., Zilla, T., Dippold, M.A., Blagodatskaya, E., Kuzyakov, Y., 2019. Microbial C:N:P stoichiometry and turnover depend on nutrients availability in soil: A ¹⁴C, ¹⁵N and ³³P triple labelling study. Soil Biology and Biochemistry131, 206–216.

[9] Chen, X.B., Hu, Y.J., Feng, S.Z., Rui, Y.C., Zhang, Z.H., He, H.B., He, X.H., Ge, T.D., Wu, J.S., Su, Y.R., 2018a. Lignin and cellulose dynamics with straw incorporation in two contrasting cropping soils. Scientific Reports8, 1633.

[10] Chen, X.B., Hu, Y.J., Xia, Y.H., Zheng, S.M., Ma, C., Rui, Y.C., He, H.B., Huang, D.Y., Zhang, Z.H., Ge, T.D., Wu, J.S., Guggenberger, G., Kuzyakov, Y., Su, Y.R., 2021. Contrasting pathways of carbon sequestration in paddy and upland soils. Global Change Biology27, 2478–2490.

[11] Chen, X.B., Xia, Y.H., Hu, Y.J., Gunina, A., Ge, T.D., Zhang, Z.H., Wu, J.S., Su, Y.R., 2018b. Effect of nitrogen fertilization on the fate of rice residue-C in paddy soil depending on depth: ¹³C amino sugar analysis. Biology and Fertility of Soils54, 523–531.

[12] Chen, X.D., Wu, J.G., Opoku-Kwanowaa, Y., 2020. Effects of returning granular corn straw on soil humus composition and humic acid structure characteristics in saline-alkali soil. Sustainability12, 1005.

[13] Chowdhury, S., Bolan, N., Farrell, M., Sarkar, B., Sarker, J.R., Kirkham, M.B., Hossain, M.Z., Kim, G.H., 2021. Role of cultural and nutrient management practices in carbon sequestration in agricultural soil. Advances in Agronomy166, 131–196.

[14] Cleveland, C.C., Liptzin, D., 2007. C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85, 235–252. DOI:10.1007/s10533–007-0533–007.

[15] Cong, P., Wang, J., Li, Y.Y., Liu, N., Dong, J.X., Pang, H.C., Zhang, L., Gao, Z.J., 2020. Changes in soil organic carbon and microbial community under varying straw incorporation strategies. Soil and Tillage Research204, 104735.

[16] Cui, Y.X., Hu, J.X., Peng, S.S., Delgado-Baquerizo, M., Moorhead, D.L., Sinsabaugh, R.L., Xu, X.F., Geyer, K.M., Fang, L.C., Smith, P., Peñuelas, J., Kuzyakov, Y., Chen, J., 2024. Limiting resources define the global pattern of soil microbial carbon use efficiency. Advanced Science11, 2308176.

[17] Duan, X., Gunina, A., Rui, Y.C., Xia, Y.H., Hu, Y.J., Ma, C., Qiao, H., Zhang, Y.M., Wu, J.S., Su, Y.R., Chen, X.B., 2024a. Contrasting processes of microbial anabolism and necromass formation between upland and paddy soils across regional scales. CATENA239, 107902.

[18] Duan, X., Rui, Y.C., Xia, Y.H., Hu, Y.J., Ma, C., Qiao, H., Zeng, G.J., Su, Y.R., Wu, J.S., Chen, X.B., 2024b. Higher microbial C use efficiency in paddy than in adjacent upland soils: evidence from continental scale. Soil and Tillage Research235, 105891.

[19] Dungait, J.A.J., Hopkins, D.W., Gregory, A.S., Whitmore, A.P., 2012. Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biology18, 1781–1796.

[20] Elrys, A.S., Uwiragiye, Y., Zhang, Y.H., Abdel-Fattah, M.K., Chen, Z.X., Zhang, H.M., Meng, L., Wang, J., Zhu, T.B., Cheng, Y., Zhang, J.B., Cai, Z.C., Chang, S.X., Müller, C., 2022. Expanding agroforestry can increase nitrate retention and mitigate the global impact of a leaky nitrogen cycle in croplands. Nature Food4, 109–121.

[21] Elrys, A.S., Wang, J., Meng, L., Zhu, Q.L., El-Sawy, M.M., Chen, Z.X., Tu, X.S., El-Saadony, M.T., Zhang, Y.H., Zhang, J.B., Cai, Z.C., Müller, C., Cheng, Y., 2023. Integrative knowledge-based nitrogen management practices can provide positive effects on ecosystem nitrogen retention. Nature Food4, 1075–1089.

[22] Engelking, B., Flessa, H., Joergensen, R.G., 2007. Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biology and Biochemistry39, 2111–2118.

[23] Fan, T., Zhang, Y.L., Hu, K.X., Xu, S.Q., Zhang, A.F., Xue, S.Q., Han, J.L., Wang, X.D., 2024. Changes in soil organic carbon and microbial community in saline soil following different forms of straw incorporation. European Journal of Soil Science75, e13457.

[24] Fang, Y.Y., Singh, B.P., Collins, D., Li, B.Z., Zhu, J., Tavakkoli, E., 2018. Nutrient supply enhanced wheat residue-carbon mineralization, microbial growth, and microbial carbon-use efficiency when residues were supplied at high rate in contrasting soils. Soil Biology and Biochemistry126, 168–178.

[25] Fang, Y.Y., Singh, B.P., Cowie, A., Wang, W.Q., Arachchi, M.H., Wang, H.L., Tavakkoli, E., 2019. Balancing nutrient stoichiometry facilitates the fate of wheat residue-carbon in physically defined soil organic matter fractions. Geoderma354, 113883.

[26] Grgas, D., Rukavina, M., Bešlo, D., Štefanac, T., Crnek, V., Šikić, T., Habuda-Stanić, M., Landeka Dragičević, T., 2023. The bacterial degradation of lignin—a review. Water15, 1272.

[27] Han, P.F., Zhang, W., Wang, G.C., Sun, W.J., Huang, Y., 2016. Changes in soil organic carbon in croplands subjected to fertilizer management: a global meta-analysis. Scientific Reports6, 27199.

[28] Han, X., Xu, C., Dungait, J.A. J., Bol, R., Wang, X.J., Wu, W.L., Meng, F.Q., 2018. Straw incorporation increases crop yield and soil organic carbon sequestration but varies under different natural conditions and farming practices in China: a system analysis. Biogeosciences15, 1933–1946.

[29] Hautala, K., Peuravuori, J., Pihlaja, K., 1997. Estimation of origin of lignin in humic dom by CuO-oxidation. Chemosphere35, 809–817.

[30] Hedges, J.I., Ertel, J.R., 1982. Characterization of lignin by gas capillary chromatography of cupric oxide oxidation products. Analytical Chemistry54, 174–178.

[31] Hicks, L.C., Lajtha, K., Rousk, J., 2021. Nutrient limitation may induce microbial mining for resources from persistent soil organic matter. Ecology102, e03328.

[32] Janusz, G., Pawlik, A., Sulej, J., Świderska-Burek, U., Jarosz-Wilkołazka, A., Paszczyński, A., 2017. Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiology Reviews41, 941–962.

[33] Jin, Z.Q., Shah, T., Zhang, L., Liu, H.Y., Peng, S.B., Nie, L.X., 2020. Effect of straw returning on soil organic carbon in rice–wheat rotation system: a review. Food and Energy Security9, e200.

[34] Joergensen, R.G., 2018. Amino sugars as specific indices for fungal and bacterial residues in soil. Biology and Fertility of Soils54, 559–568.

[35] Kästner, M., Miltner, A., Thiele-Bruhn, S., Liang, C., 2021. Microbial necromass in soils—linking microbes to soil processes and carbon turnover. Frontiers in Environmental Science9, 756378.

[36] Kirkby, C.A., Richardson, A.E., Wade, L.J., Batten, G.D., Blanchard, C., Kirkegaard, J.A., 2013. Carbon-nutrient stoichiometry to increase soil carbon sequestration. Soil Biology and Biochemistry60, 77–86.

[37] Kulmatiski, A., Beard, K.H., 2008. Decoupling plant-growth from land-use legacies in soil microbial communities. Soil Biology and Biochemistry40, 1059–1068.

[38] Li, B.Z., Liang, F., Wang, Y.J., Cao, W.C., Song, H., Chen, J.S., Guo, J.H., 2023. Magnitude and efficiency of straw return in building up soil organic carbon: a global synthesis integrating the impacts of agricultural managements and environmental conditions. Science of the Total Environment875, 162670.

[39] Li, J., Zhang, X.C., Luo, J.F., Lindsey, S., Zhou, F., Xie, H.T., Li, Y., Zhu, P., Wang, L.C., Shi, Y.L., He, H.B., Zhang, X.D., 2020. Differential accumulation of microbial necromass and plant lignin in synthetic versus organic fertilizer-amended soil. Soil Biology and Biochemistry149, 107967.

[40] Liang, C., Amelung, W., Lehmann, J., Kästner, M., 2019. Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology25, 3578–3590.

[41] Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology2, 17105.

[42] Malik, A.A., Puissant, J., Buckeridge, K.M., Goodall, T., Jehmlich, N., Chowdhury, S., Gweon, H.S., Peyton, J.M., Mason, K.E., Van Agtmaal, M., Blaud, A., Clark, I.M., Whitaker, J., Pywell, R.F., Ostle, N., Gleixner, G., Griffiths, R.I., 2018. Land use driven change in soil pH affects microbial carbon cycling processes. Nature Communications9, 3591.

[43] Meng, X.T., Zhang, X.C., Li, Y.N., Jiao, Y.P., Fan, L.C., Jiang, Y.J., Qu, C.Y., Filimonenko, E., Jiang, Y.H., Tian, X.H., Shi, J.L., Kuzyakov, Y., 2024. Nitrogen fertilizer builds soil organic carbon under straw return mainly via microbial necromass formation. Soil Biology and Biochemistry188, 109223.

[44] Mo, F., Yang, D.Y., Wang, X.K., Crowther, T.W., Vinay, N., Luo, Z.K., Yu, K.L., Sun, S.K., Zhang, F., Xiong, Y.C., Liao, Y.C., 2024. Nutrient limitation of soil organic carbon stocks under straw return. Soil Biology and Biochemistry192, 109360.

[45] Moore-Kucera, J., Dick, R.P., 2008. Application of ¹³C-labeled litter and root materials for in situ decomposition studies using phospholipid fatty acids. Soil Biology and Biochemistry40, 2485–2493.

[46] Mooshammer, M., Wanek, W., Hämmerle, I., Fuchslueger, L., Hofhansl, F., Knoltsch, A., Schnecker, J., Takriti, M., Watzka, M., Wild, B., Keiblinger, K.M., Zechmeister-Boltenstern, S., Richter, A., 2014. Adjustment of microbial nitrogen use efficiency to carbon: nitrogen imbalances regulates soil nitrogen cycling. Nature Communications5, 3694.

[47] Pan, G.X., Smith, P., Pan, W.N., 2009. The role of soil organic matter in maintaining the productivity and yield stability of cereals in China. Agriculture, Ecosystems & Environment129, 344–348.

[48] Qiu, J.J., Wang, L.G., Li, H., Tang, H.J., Li, C.S., Van Ranst, E., 2009. Modeling the impacts of soil organic carbon content of croplands on crop yields in China. Agricultural Sciences in China8, 464–471.

[49] Spohn, M., Klaus, K., Wanek, W., Richter, A., 2016. Microbial carbon use efficiency and biomass turnover times depending on soil depth–Implications for carbon cycling. Soil Biology and Biochemistry96, 74–81.

[50] Wu, H.L., Cai, A.D., Xing, T.T., Huai, S.C., Zhu, P., Han, X.Z., Xu, M.G., Lu, C.A., 2022. Integrated management of crop residue and nutrient enhances new carbon formation by regulating microbial taxa and enzymes. Journal of Integrative Agriculture21, 1772–1785.

[51] Yu, F., Zhang, W.L., Hou, X., Li, Y., Tong, J.X., 2023. How nutrient loads influence microbial-derived carbon accumulation in wetlands: a new insight from microbial metabolic investment strategies. Environmental Research217, 114981.

[52] Yu, M.J., Su, W.Q., Huang, L.B., Parikh, S.J., Tang, C.X., Dahlgren, R.A., Xu, J.M., 2021. Bacterial community structure and putative nitrogen-cycling functional traits along a charosphere gradient under waterlogged conditions. Soil Biology and Biochemistry162, 108420.

[53] Zhang, X.D., Amelung, W., 1996. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology and Biochemistry28, 1201–1206.

[54] Zheng, S.M., Xia, Y.H., Hu, Y.J., Chen, X.B., Rui, Y.C., Gunina, A., He, X.Y., Ge, T.D., Wu, J.S., Su, Y.R., Kuzyakov, Y., 2021. Stoichiometry of carbon, nitrogen, and phosphorus in soil: Effects of agricultural land use and climate at a continental scale. Soil and Tillage Research209, 104903.

[55] Zhu, Z.K., Fang, Y.Y., Liang, Y.Q., Li, Y.H., Liu, S.L., Li, Y.F., Li, B.Z., Gao, W., Yuan, H.Z., Kuzyakov, Y., Wu, J.S., Richter, A., Ge, T.D., 2022. Stoichiometric regulation of priming effects and soil carbon balance by microbial life strategies. Soil Biology and Biochemistry169, 108669.

Declaration of competing interest

The authors declare no competing interests.

Acknowledgements

This work was financially supported by the National Key R&D Program of China (Grant No. 2021YFD1901203), the National Natural Science Foundation of China (Grant Nos. 42377348, 42177295), and the Science Foundation for Distinguished Young Scholars of Hunan Province (Grant No. 2024JJ2052).

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-024-0284-9 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2024 Higher Education Press