Elevational control on microbial residues contributions to soil organic carbon: Dual regulation by soil moisture and total nitrogen dynamics in semi-arid mountain soils

Abstract

Microbial residues carbon (MRC) plays a key role in shaping soil organic carbon (SOC) composition, but there is still no consensus on the pattern of elevational contribution of microbial residues to SOC. Utilizing biomarker amino sugars, this study quantified MRC accumulation and its contribution to SOC sequestration along an elevational gradient. Results showed that MRC concentrations increased significantly with increasing elevation, but their proportionate contribution to SOC showed a paradoxical decrease. MRC accounted for 50.47% of the SOC, including fungal residue carbon (FRC; 38.26%) and bacterial residue carbon (BRC; 12.21%). These results suggest that FRC consistently dominates the contribution of MRC to SOC. Although both FRC and BRC demonstrated similar elevational trends in their absolute accumulation, their accumulation mechanisms were distinctly regulated by environmental factors. BRC accumulation was directly dependent on soil total nitrogen (TN) and soil water content (SWC). In contrast, FRC accumulation was predominantly regulated by SWC alone. The overarching influence of elevation was primarily indirect, mediated through its effects on key soil properties, particularly nitrogen (N) availability and moisture conditions (SWC). This indicates that elevational gradients shape the patterns of microbial residue accumulation and their fractional contribution to SOC largely by modulating N and water availability. These finding provide crucial mechanistic insights into microbial-mediated SOC persistence under changing environmental conditions. The differential controls on fungal versus bacterial residue incorporation underscore the need to account for microbial community composition and their distinct environmental sensitivities in biogeochemical models. Incorporating elevational gradients and their influence on N and moisture dynamics is therefore essential for accurately projecting terrestrial carbon cycling responses to global climate change.

Graphical abstract

Keywords

elevation / amino sugars / microbial residues / soil organic carbon / semi-arid mountains

Highlight

	● The content of microbial residues C increased along an elevation gradient.
	● The contribution of microbial residue C to SOC decreased along the elevation gradient.
	● Fungal residue C contributes more significantly to SOC than bacterial residue C.
	● Elevation affects accumulation of microbial residues C and their contribution to SOC.
	● TN and SWC are primarily limited factors of accumulation of microbial residues C.

References

[1] Appuhn, A., Joergensen, R.G., 2006. Microbial colonisation of roots as a function of plant species. Soil Biology and Biochemistry38, 1040–1051.

[2] Bach, E.M., Baer, S.G., Meyer, C.K., Six, J., 2010. Soil texture affects soil microbial and structural recovery during grassland restoration. Soil Biology and Biochemistry42, 2182–2191.

[3] Bao, S.D., 2000. Soil Agricultural Chemical Analysis. 3rd ed. Beijing: China Agricultural Press.

[4] Baumert, V.L., Forstner, S.J., Zethof, J.H.T., Vogel, C., Heitkötter, J., Schulz, S., Kögel-Knabner, I., Mueller, C.W., 2021. Root-induced fungal growth triggers macroaggregation in forest subsoils. Soil Biology and Biochemistry157, 108244.

[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] Brockett, B.F.T., Prescott, C.E., Grayston, S.J., 2012. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biology and Biochemistry44, 9–20.

[7] Browne, M.W., Cudeck, R., 1993. Alternative ways of assessing model fit. In: Bollen, K.A., Long, J.S., eds. Testing Structural Equation Models. Newbury Park136–162.

[8] Cao, Y.F., Ding, J.Z., Li, J., Xin, Z.M., Ren, S., Wang, T., 2023. Necromass-derived soil organic carbon and its drivers at the global scale. Soil Biology and Biochemistry181, 109025.

[9] Chen, G.P., Ma, S.H., Tian, D., Xiao, W., Jiang, L., Xing, A.J., Zou, A.L., Zhou, L.H., Shen, H.H., Zheng, C.Y., Ji, C.J., He, H.B., Zhu, B., Liu, L.L., Fang, J.Y., 2020. Patterns and determinants of soil microbial residues from tropical to boreal forests. Soil Biology and Biochemistry151, 108059.

[10] Clemmensen, K.E., Bahr, A., Ovaskainen, O., Dahlberg, A., Ekblad, A., Wallander, H., Stenlid, J., Finlay, R.D., Wardle, D.A., Lindahl, B.D., 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science339, 1615–1618.

[11] Davidson, E.A., Samanta, S., Caramori, S.S., Savage, K., 2012. The Dual Arrhenius and Michaelis-Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Global Change Biology18, 371–384.

[12] Delgado-Baquerizo, M., Maestre, F.T., Gallardol, A., Bowker, M.A., Wallenstein, M.D., Quero, J.L., Ochoa, V., Gozalo, B., Garcia-Gomez, M., Soliveres, S., García-Palacios, P., Berdugo, M., Valencia, E., Escolar, C., Arredondo, T., Barraza-Zepeda, C., Bran, D., Carreira, J.A., Chaieb, M., Conceição, A.A., Derak, M., Eldridge, D.J., Escudero, A., Espinosa, C.I., Gaitán, J., Gatica, M.G., Gómez-González, S., Guzman, E., Gutiérrez, J.R., Florentino, A., Hepper, E., Hernández, R.M., Huber-Sannwald, E., Jankju, M., Liu, J.,Mau, R.L., Miriti, M., Monerris, J., Naseri, K., Noumi, Z., Polo, V., Prina, A., Pucheta, E., Ramírez, E., Ramírez-Collantes, D.A., Romão, R., Tighe, M., Torres, D., Torres-Díaz, C., Ungar, E.D., Val, J., Wamiti, W.,Wang, D., Zaady, E., 2013. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature502, 672–676.

[13] Deng, F.B., Liang, C., 2022. Revisiting the quantitative contribution of microbial necromass to soil carbon pool: stoichiometric control by microbes and soil. Soil Biology and Biochemistry165, 108486.

[14] Deng, S.J., Wang, Q.T., Wang, D.G., Yang, H., Zhang, P.P., Li, N., Zhang, X.J., Wang, R.H., Yin, H.J., 2024. The accumulation capacity of microbial residues in the rhizosphere increased along an elevation gradient. CATENA238, 107891.

[15] 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.

[16] Eswaran, H., van den Berg, E., Reich, P., 1993. Organic carbon in soils of the world. Soil Science Society of America Journal57, 192–194.

[17] Fanin, N., Kardol, P., Farrell, M., Nilsson, M.C., Gundale, M.J., Wardle, D.A., 2019. The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biology and Biochemistry128, 111–114.

[18] Fernandez, C.W., Langley, J.A., Chapman, S., McCormack, M.L., Koide, R.T., 2016. The decomposition of ectomycorrhizal fungal necromass. Soil Biology and Biochemistry93, 38–49.

[19] Fierer, N., Schimel, J.P., Holden, P.A., 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology and Biochemistry35, 167–176.

[20] Frostegård, A., Bååth, E., 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils22, 59–65.

[21] He, H.B., Zhang, W., Zhang, X.D., Xie, H.T., Zhuang, J., 2011. Temporal responses of soil microorganisms to substrate addition as indicated by amino sugar differentiation. Soil Biology and Biochemistry43, 1155–1161.

[22] He, M., Fang, K., Chen, L.Y., Feng, X.H., Qin, S.Q., Kou, D., He, H.B., Liang, C., Yang, Y.H., 2022. Depth-dependent drivers of soil microbial necromass carbon across Tibetan alpine grasslands. Global Change Biology28, 936–949.

[23] He, X.J., Liu, F.B., Ma, T., Ma, A.S., Wang, Y.Y., Li, Y.F., Gao, W.J., Yang, Z.Y., Ke, J.S., Xiao, Y., Zhang, L., Liu, M., Liu, X., 2025. Temperature and microbial metabolic limitations govern microbial carbon use efficiency in the Tibetan alpine grassland. Applied Soil Ecology206, 105880.

[24] Hou, Z.N., Wang, R.H., Chang, S., Zheng, Y., Ma, T.T., Xu, S.Q., Zhang, X.J., Shi, X., Lu, J., Luo, D.Q., Wang, B., Du, Z.L., Wei, Y.Q., 2024. The contribution of microbial necromass to soil organic carbon and influencing factors along a variation of habitats in alpine ecosystems. Science of the Total Environment921, 171126.

[25] Hu, Y.T., Zheng, Q., Noll, L., Zhang, S.S., Wanek, W., 2020. Direct measurement of the in situ decomposition of microbial-derived soil organic matter. Soil Biology and Biochemistry141, 107660.

[26] Huang, Y., Liang, C., Duan, X.W., Chen, H., Li, D.J., 2019. Variation of microbial residue contribution to soil organic carbon sequestration following land use change in a subtropical karst region. Geoderma353, 340–346.

[27] Inglett, K.S., Inglett, P.W., Reddy, K.R., 2011. Soil microbial community composition in a restored calcareous subtropical wetland. Soil Science Society of America Journal75, 1731–1740.

[28] IPCC, 2023. Sixth Assessment Report, Climate Change 2023: Synthesis Report. .

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

[30] Kallenbach, C.M., Frey, S.D., Grandy, A.S., 2016. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nature Communications7, 13630.

[31] Kindler, R., Miltner, A., Richnow, H.H., Kästner, M., 2006. Fate of gram-negative bacterial biomass in soil—mineralization and contribution to SOM. Soil Biology and Biochemistry38, 2860–2870.

[32] Landesman, W.J., Dighton, J., 2010. Response of soil microbial communities and the production of plant-available nitrogen to a two-year rainfall manipulation in the New Jersey Pinelands. Soil Biology and Biochemistry42, 1751–1758.

[33] Lehmann, J., Kleber, M., 2015. The contentious nature of soil organic matter. Nature528, 60–68.

[34] Li, L.D., Wilson, C.B., He, H.B., Zhang, X.D., Zhou, F., Schaeffer, S.M., 2019. Physical, biochemical, and microbial controls on amino sugar accumulation in soils under long-term cover cropping and no-tillage farming. Soil Biology and Biochemistry135, 369–378.

[35] Li, Y.Q., Wang, X.Y., Mou, X.M., Jia, B., Lian, J., Niu, Y.Y., Gong, X.W., Li, Y.Q., 2025. Divergent mechanisms driving microbial necromass in topsoil and subsoil along an altitudinal gradient on the Loess Plateau. Geoderma457, 117311.

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

[37] Liang, C., Balser, T.C., 2012. Warming and nitrogen deposition lessen microbial residue contribution to soil carbon pool. Nature Communications3, 1222.

[38] Liang, C., Cheng, G., Wixon, D.L., Balser, T.C., 2011. An absorbing Markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry106, 303–309.

[39] Liang, C., Gutknecht, J.L.M., Balser, T.C., 2015. Microbial lipid and amino sugar responses to long-term simulated global environmental changes in a California annual grassland. Frontiers in Microbiology6, 385.

[40] Liang, C., Kästner, M., Joergensen, R.G., 2020. Microbial necromass on the rise: the growing focus on its role in soil organic matter development. Soil Biology and Biochemistry150, 108000.

[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] Liu, D., Zhou, Z.Y., Iqbal, S., Dou, T.T., Bonito, G., Liu, W., An, S.S., Chater, C.C. C., Perez-Moreno, J., Che, R.X., Jones, D.L., Yu, F.Q., 2024. Fungal necromass contribution to carbon sequestration in global croplands: a meta-analysis of driving factors and conservation practices. Science of the Total Environment949, 174954.

[43] Liu, H., Ren, F.R., Wan, S.Q., Han, S.J., Zheng, J.Q., 2025. Nitrogen and water additions with or without mowing altered soil microbial community characteristics in a semi-arid steppe. Ecological Processes14, 3.

[44] Liu, Y., He, N.P., Zhu, J.X., Xu, L., Yu, G.R., Niu, S.L., Sun, X.M., Wen, X.F., 2017. Regional variation in the temperature sensitivity of soil organic matter decomposition in China's forests and grasslands. Global Change Biology23, 3393–3402.

[45] Luo, Z.Y., Ren, J.N., Manzoni, S., Fatichi, S., 2024. Temperature controls the relation between soil organic carbon and microbial carbon use efficiency. Global Change Biology30, e17492.

[46] Ma, T., Zhu, S.S., Wang, Z.H., Chen, D.M., Dai, G.H., Feng, B.W., Su, X.Y., Hu, H.F., Li, K.H., Han, W.X., Liang, C., Bai, Y.F., Feng, X.J., 2018. Divergent accumulation of microbial necromass and plant lignin components in grassland soils. Nature Communications9, 3480.

[47] Maestre, F.T., Delgado-Baquerizo, M., Jeffries, T.C., Eldridge, D.J., Ochoa, V., Gozalo, B., Quero, J.L., García-Gómez, M., Gallardo, A., Ulrich, W., Bowker, M.A., Arredondo, T., Barraza-Zepeda, C., Bran, D., Florentino, A., Gaitán, J., Gutiérrez, J.R., Huber-Sannwald, E., Jankju, M., Mau, R.L., Miriti, M., Naseri, K., Ospina, A., Stavi, I., Wang, D.L., Woods, N.N., Yuan, X., Zaady, E., Singh, B.K., 2015. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proceedings of the National Academy of Sciences of the United States of America112, 15684–15689.

[48] Mou, Z.J., Kuang, L.H., He, L.F., Zhang, J., Zhang, X.Y., Hui, D.F., Li, Y., Wu, W.J., Mei, Q.M., He, X.J., Kuang, Y.W., Wang, J., Wang, Y.Q., Lambers, H., Sardans, J., Peñuelas, J., Liu, Z.F., 2021. Climatic and edaphic controls over the elevational pattern of microbial necromass in subtropical forests. CATENA207, 105707.

[49] Sampedro, L., Jeannotte, R., Whalen, J.K., 2006. Trophic transfer of fatty acids from gut microbiota to the earthworm Lumbricus terrestris L. Soil Biology and Biochemistry38, 2188–2198.

[50] Schweigert, M., Herrmann, S., Miltner, A., Fester, T., Kästner, M., 2015. Fate of ectomycorrhizal fungal biomass in a soil bioreactor system and its contribution to soil organic matter formation. Soil Biology and Biochemistry88, 120–127.

[51] Siles, J.A., Cajthaml, T., Filipová, A., Minerbi, S., Margesin, R., 2017. Altitudinal, seasonal and interannual shifts in microbial communities and chemical composition of soil organic matter in Alpine forest soils. Soil Biology and Biochemistry112, 1–13.

[52] Sradnick, A., Oltmanns, M., Raupp, J., Joergensen, R.G., 2014. Microbial residue indices down the soil profile after long-term addition of farmyard manure and mineral fertilizer to a sandy soil. Geoderma226–227, 79–84.

[53] Struecker, J., Joergensen, R.G., 2015. Microorganisms and their substrate utilization patterns in topsoil and subsoil layers of two silt loams, differing in soil organic C accumulation due to colluvial processes. Soil Biology and Biochemistry91, 310–317.

[54] Sun, H.Y., Koal, P., Liu, D., Gerl, G., Schroll, R., Gattinger, A., Joergensen, R.G., Munch, J.C., 2016. Soil microbial community and microbial residues respond positively to minimum tillage under organic farming in Southern Germany. Applied Soil Ecology108, 16–24.

[55] Sundqvist, M.K., Sanders, N.J., Wardle, D.A., 2013. Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annual Review of Ecology, Evolution, and Systematics44, 261–280.

[56] Wang, B.R., An, S.S., Liang, C., Liu, Y., Kuzyakov, Y., 2021. Microbial necromass as the source of soil organic carbon in global ecosystems. Soil Biology and Biochemistry162, 108422.

[57] Wang, B.R., Huang, Y.M., Li, N., Yao, H.J., Yang, E., Soromotin, A.V., Kuzyakov, Y., Cheptsov, V., Yang, Y., An, S.S., 2022a. Initial soil formation by biocrusts: nitrogen demand and clay protection control microbial necromass accrual and recycling. Soil Biology and Biochemistry167, 108607.

[58] Wang, C.Y., Li, X.Y., Zhang, M., Han, Z.C., Xia, Y., Lian, P.P., Yang, L.M., Yue, K., Fan, Y.X., 2024. Nitrogen deposition enhances accumulation of microbial and plant-derived carbon in forest soils: a global meta-analysis. Plant and Soil505, 465–478.

[59] Wang, Q.T., Zhang, Z.L., Zhu, X.M., Liu, Z.F., Li, N., Xiao, J., Liu, Q., Yin, H.J., 2022b. Absorptive roots drive a larger microbial carbon pump efficacy than transport roots in alpine coniferous forests. Journal of Ecology110, 1646–1655.

[60] Whalen, E.D., Grandy, A.S., Sokol, N.W., Keiluweit, M., Ernakovich, J., Smith, R.G., Frey, S.D., 2022. Clarifying the evidence for microbial- and plant-derived soil organic matter, and the path toward a more quantitative understanding. Global Change Biology28, 7167–7185.

[61] Wu, G.P., Huang, G., Lin, S.N., Huang, Z.Y., Cheng, H., Su, Y.G., 2024. Changes in soil organic carbon stocks and its physical fractions along an elevation in a subtropical mountain forest. Journal of Environmental Management351, 119823.

[62] Wu, M.Y., Chen, L., Ma, J.P., Zhang, Y.Q., Li, X.B., Pang, D.B., 2023. Aggregate-associated carbon contributes to soil organic carbon accumulation along the elevation gradient of Helan Mountains. Soil Biology and Biochemistry178, 108926.

[63] Wu, Y., Chen, W.J., Entemake, W., Wang, J., Liu, H.F., Zhao, Z.W., Li, Y.Z., Qiao, L.L., Yang, B., Liu, G.B., Xue, S., 2021. Long-term vegetation restoration promotes the stability of the soil micro-food web in the Loess Plateau in North-west China. CATENA202, 105293.

[64] Yang, L.M., Lyu, M., Li, X.J., Xiong, X.L., Lin, W.S., Yang, Y.S., Xie, J.S., 2020. Decline in the contribution of microbial residues to soil organic carbon along a subtropical elevation gradient. Science of the Total Environment749, 141583.

[65] Zeng, L., He, X.J., Zhu, G.Y., Zhou, L.H., Luo, M., Yin, X.H., Long, Y.X., Dai, J.L., Ouyang, X., Yang, Y.C., 2023. Bedrock and climate jointly control microbial necromass along a subtropical elevational gradient. Applied Soil Ecology189, 104902.

[66] Zeng, X.M., Feng, J., Yu, D.L., Wen, S.H., Zhang, Q.G., Huang, Q.Y., Delgado-Baquerizo, M., Liu, Y.R., 2022. Local temperature increases reduce soil microbial residues and carbon stocks. Global Change Biology28, 6433–6445.

[67] Zhang, B., Liang, C., He, H.B., Zhang, X.D., 2013. Variations in soil microbial communities and residues along an altitude gradient on the northern slope of Changbai Mountain, China. PLoS One8, e66184.

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

[69] Zhao, Z.W., Qin, Y.L., Wu, Y., Chen, W.J., Wang, H., Chen, J.W., Yang, J.Q., Liu, G.B., Xue, S., 2025. Microbial necromass carbon drives soil organic carbon accumulation during long-term vegetation succession. Journal of Applied Ecology62, 932–944.

[70] Zheng, H.F., Heděnec, P., Rousk, J., Schmidt, I.K., Peng, Y., Vesterdal, L., 2022. Effects of common European tree species on soil microbial resource limitation, microbial communities and soil carbon. Soil Biology and Biochemistry172, 108754.

[71] Zhou, X.Q., Guo, Z.Y., Chen, C.R., Jia, Z.J., 2017. Soil microbial community structure and diversity are largely influenced by soil pH and nutrient quality in 78-year-old tree plantations. Biogeosciences14, 2101–2111.

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