Managing above-ground plant carbon inputs can pave the way toward carbon neutrality and mitigating climate change. Chemical complexity of plant residues largely controls carbon sequestration. There exist conflicting opinions on whether residue chemistry diverges or converges after long-term decomposition. Moreover, whether and how microbial communities regulate residue chemistry remains unclear. This study investigated the decomposition processes and residue composition dynamics of maize straw and wheat straw and related microbiomes over a period of 9 years in three climate zones. Residue chemistry exhibited a divergent-convergent trajectory during decomposition, that is, the residue composition diverged during the 0.5–3 year period under the combined effect of straw type and climate and then converged to an array of common compounds during the 3–9 year period. Chemical divergence during the first 2–3 years was primarily driven by the changes in extracellular enzyme activity influenced by keystone taxa-guided bacterial networks, and the keystone taxa belonged to Alphaproteobacteria, particularly Rhizobiales. After 9 years, microbial assimilation became dominant, leading to chemical convergence, and fungi, particularly Chaetomium, were the main contributors to microbial assimilation. Overall, this study demonstrated that keystone taxa regulate the divergent-convergent trajectory in residue chemistry.
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MiSeq sequencing data and metagenomic sequencing data have been deposited in the NCBI Sequence Read Archive under the SRA accessions of SRP312985 and SRP417783, respectively. All other data generated or analyzed during this study are included in this article and/or its supplementary information files.
Lal R, Bruce JP. The potential of world cropland soils to sequester C and mitigate the greenhouse effect. Environ Sci Policy. 1999;2:177–85.
Wang J, Feng L, Palmer PI, Liu Y, Fang S, Bosch H, et al. Large Chinese land carbon sink estimated from atmospheric carbon dioxide data. Nature. 2020;586:720–3.
Lal R. Managing soils and ecosystems for mitigating anthropogenic carbon emissions and advancing global food security. Bioscience. 2010;60:708–21.
Rumpel C, Lehmann J, Chabbi A. ‘4 per 1,000’ initiative will boost soil carbon for climate and food security. Nature. 2018;553:27–27.
Zhao Y, Wang M, Hu S, Zhang X, Ouyang Z, Zhang G, et al. Economics- and policy-driven organic carbon input enhancement dominates soil organic carbon accumulation in Chinese croplands. Proc Natl Acad Sci USA. 2018;115:4045–50.
Yang F, Xu Y, Cui Y, Meng Y, Dong Y, Li R, et al. Variation of soil organic matter content in croplands of china over the last three decades (in Chinese). Acta Pedol Sin. 2017;5:1047–56.
Lehmann J, Hansel CM, Kaiser C, Kleber M, Maher K, Manzoni S, et al. Persistence of soil organic carbon caused by functional complexity. Nat Geosci. 2020;13:529–34.
Schmidt M, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA. et al. Persistence of soil organic matter as an ecosystem property. Nature. 2011;478:49–56.
Lehmann J, Kleber M. The contentious nature of soil organic matter. Nature. 2015;528:60–68.
Cotrufo MF, Soong JL, Horton AJ, Campbell EE, Haddix ML, Wall DH, et al. Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci. 2015;8:776–9.
Schnitzer M, Monreal CM. Quo vadis soil organic matter research? A biological link to the chemistry of humification. Adv Agron. 2011;113:139–213.
Wang X, Sun B, Mao J, Sui Y, Cao X. Structural convergence of maize and wheat straw during two-year decomposition under different climate conditions. Environ Sci Technol. 2012;46:7159–65.
Liang C, Schimel JP, Jastrow JD. The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol. 2017;2:17105.
Wickings K, Grandy AS, Reed SC, Cleveland CC. The origin of litter chemical complexity during decomposition. Ecol Lett. 2012;15:1180–8.
Grandy AS, Neff JC. Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ. 2008;404:297–307.
Jenkinson DS, Ayanaba A. Decomposition of 14C labeled plant material under tropical conditions. Soil Sci Soc Am J. 1977;41:912–5.
Li Y, Chen N, Harmon ME, Li Y, Cao X, Chappell MA, et al. Plant species rather than climate greatly alters the temporal pattern of litter chemical composition during long-term decomposition. Sci Rep. 2015;5:15783.
Preston CM, Nault JR, Trofymow JA, Smyth C, Grp CW. Chemical changes during 6 years of decomposition of 11 litters in some Canadian forest sites. Part 1. Elemental composition, tannins, phenolics, and proximate fractions. Ecosystems. 2009;12:1053–77.
Kallenbach CM, Frey SD, Grandy AS. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun. 2016;7:13630.
Wickings K, Stuart Grandy A, Reed S, Cleveland C. Management intensity alters decomposition via biological pathways. Biogeochemistry. 2011;104:365–79.
Schimel JP, Schaeffer SM. Microbial control over carbon cycling in soil. Front Microbiol. 2012;3:348.
Sun B, Wang X, Wang F, Jiang Y, Zhang X-X. Assessing the relative effects of geographic location and soil type on microbial communities associated with straw decomposition. Appl Environ Microbiol. 2013;79:3327.
Balser TC, Firestone MK. Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry. 2005;73:395–415.
Grandy AS, Neff JC, Weintrau MN. Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem. 2007;39:2701–11.
Maynard DS, Crowther TW, Bradford MA. Competitive network determines the direction of the diversity-function relationship. Proc Natl Acad Sci USA. 2017;114:11464–9.
Wagg C, Bender SF, Widmer F, van der Heijden MGA. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA. 2014;111:5266–70.
Snajdr J, Cajthaml T, Valaskova V, Merhautova V, Petrankova M, Spetz P, et al. Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiol Ecol. 2011;75:291–303.
Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol Biochem. 2016;97:188–98.
Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.
Carrias J-F, Gerphagnon M, Rodríguez-Pérez H, Borrel G, Loiseau C, Corbara B, et al. Resource availability drives bacterial succession during leaf-litter decomposition in a bromeliad ecosystem. FEMS Microbiol Ecol. 2020;96:fiaa045.
Zhan P, Liu Y, Wang H, Wang C, Xia M, Wang N, et al. Plant litter decomposition in wetlands is closely associated with phyllospheric fungi as revealed by microbial community dynamics and co-occurrence network. Sci Total Environ. 2021;753:142194.
Panettieri M, Knicker H, Murillo JM, Madejon E, Hatcher PG. Soil organic matter degradation in an agricultural chronosequence under different tillage regimes evaluated by organic matter pools, enzymatic activities and CPMAS C-13 NMR. Soil Biol Biochem. 2014;78:170–81.
Skjemstad JO, Clarke P, Taylor JA, Oades JM, Newman RH. The removal of magnetic-materials from surface soils - a solid state 13C CP/MAS NMR study. Aust J Soil Res. 1994;32:1215–29.
Sokolenko S, Jézéquel T, Hajjar G, Farjon J, Akoka S, Giraudeau P. Robust 1D NMR lineshape fitting using real and imaginary data in the frequency domain. J Magn Reson. 2019;298:91–100.
Grandy AS, Strickland MS, Lauber CL, Bradford MA, Fierer N. The influence of microbial communities, management, and soil texture on soil organic matter chemistry. Geoderma.2009;150:278–86.
Saiya-Cork KR, Sinsabaugh RL, Zak DR. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem. 2002;34:1309–15.
Allison SD, Jastrow JD. Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem. 2006;38:3245–56.
Zhang XD, Amelung W. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol Biochem. 1996;28:1201–6.
Lee CK, Barbier BA, Bottos EM, McDonald IR, Cary SC. The inter-valley soil comparative survey: the ecology of dry valley edaphic microbial communities. ISME J. 2012;6:1046–57.
Degnan PH, Ochman H. Illumina-based analysis of microbial community diversity. ISME J. 2012;6:183–94.
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35:7188–96.
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22:5271–7.
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, et al. Microbial co-occurrence relationships in the human microbiome. PLoS Comp Biol. 2012;8:e1002606.
Chong IG, Jun CH. Performance of some variable selection methods when multicollinearity is present. Chemometrics Intell Lab Syst. 2005;78:103–12.
Strukelj M, Brais S, Mazerolle MJ, Pare D, Drapeau P. Decomposition patterns of foliar litter and deadwood in managed and unmanaged stands: A 13-year experiment in boreal mixedwoods. Ecosystems. 2018;21:68–84.
Manzoni S, Piñeiro G, Jackson RB, Jobbágy EG, Kim JH, Porporato A. Analytical models of soil and litter decomposition: Solutions for mass loss and time-dependent decay rates. Soil Biol Biochem. 2012;50:66–76.
Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14:927–30.
Grace JB (ed). Structural Equation Modeling and Natural Systems. Cambridge University Press, Cambridge, 2006.
Shen Y, Cheng R, Xiao W, Yang S, Guo Y, Wang N, et al. Labile organic carbon pools and enzyme activities of Pinus massoniana plantation soil as affected by understory vegetation removal and thinning. Sci Rep. 2018;8:573.
Gallo ME, Lauber CL, Cabaniss SE, Waldrop MP, Sinsabaugh RL, Zak DR. Soil organic matter and litter chemistry response to experimental N deposition in northern temperate deciduous forest ecosystems. Glob Change Biol. 2005;11:1514–21.
Wilhelm RC, Singh R, Eltis LD, Mohn WW. Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing. ISME J. 2019;13:413–29.
Sahay H, Yadav AN, Singh AK, Singh S, Kaushik R, Saxena AK. Hot springs of Indian Himalayas: potential sources of microbial diversity and thermostable hydrolytic enzymes. 3 Biotech. 2017;7:118.
Robledo M, Rivera L, Jimenez-Zurdo JI, Rivas R, Dazzo F, Velazquez E, et al. Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces. Micro Cell Factories. 2012;11:125.
Wang X, Bian Q, Jiang Y, Zhu L, Chen Y, Liang Y, et al. Organic amendments drive shifts in microbial community structure and keystone taxa which increase C mineralization across aggregate size classes. Soil Biol Biochem. 2021;153:108062.
Joergensen RG. Amino sugars as specific indices for fungal and bacterial residues in soil. Biol Fert Soils. 2018;54:559–68.
Chen Y, Sun R, Sun T, Chen P, Yu Z, Ding L, et al. Evidence for involvement of keystone fungal taxa in organic phosphorus mineralization in subtropical soil and the impact of labile carbon. Soil Biol Biochem. 2020;148:107900.
Puentes-Tellez PE, Salles JF. Construction of effective minimal active microbial consortia for lignocellulose degradation. Micro Ecol. 2018;76:419–29.
Zark M, Dittmar T. Universal molecular structures in natural dissolved organic matter. Nat Commun. 2018;9:3178.
Lynch LM, Sutfin NA, Fegel TS, Boot CM, Covino TP, Wallenstein MD. River channel connectivity shifts metabolite composition and dissolved organic matter chemistry. Nat Commun. 2019;10:459.
Filley TR, Boutton TW, Liao JD, Jastrow JD, Gamblin DE. Chemical changes to nonaggregated particulate soil organic matter following grassland-to-woodland transition in a subtropical savanna. J Geophys Res Biogeosci. 2008;113:G03009.
Stewart CE, Neff JC, Amatangelo KL, Vitousek PM. Vegetation effects on soil organic matter chemistry of aggregate fractions in a Hawaiian forest. Ecosystems. 2011;14:382–97.
We gratefully thank Dr. Xudong Zhang’s lab for their assistance in amino sugar analysis. We appreciate the experiment management and sampling assistance from staffs in Hailun, Fengqiu and Yingtan Research Stations. This work is financially supported by the National Key R&D Program (2022YFD1900600), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA28030102), the Science Foundation of the Chinese Academy of Sciences (ISSASIP2211), National Natural Science Foundation of China (31930070), and the China Agriculture Research System of MOF and MARA (CARS-22, CARS-52).
The authors declare no competing interests.
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Wang, X., Liang, C., Mao, J. et al. Microbial keystone taxa drive succession of plant residue chemistry. ISME J 17, 748–757 (2023). https://doi.org/10.1038/s41396-023-01384-2