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Litter quality controls the contribution of microbial carbon to main microbial groups and soil organic carbon during its decomposition

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Abstract

A 163-day decomposition experiment with 13C-enriched leaf litter of Populus davidiana (low quality, with low N content, high C:N and high lignin content) and Quercus wutaishanica (high quality, with high N content, low C:N and low lignin content) was conducted to investigate the effects of litter quality on the microbial contribution to soil organic C (SOC). We used stable isotope probing (SIP) technology of phospholipid fatty acid (PLFA) and amino sugar, determined soil enzyme activities, and microbial C use efficiency (CUE) to study the microbial contribution to SOC formation as affected by litter quality. Gram-positive (G +) and Gram-negative (G −) bacteria rapidly assimilated the readily available C of high- and low-quality litter, whereas fungi selectively utilized more recalcitrant compounds. The ratio of 13C-fungal to 13C-bacterial necromass increased and then leveled off until the end of the incubation for both litters. Therefore, litter-derived C was first utilized by bacteria, then allocated presumably by the consumption of bacterial necromass to fungi, and, at the end, the litter C was mainly stabilized as fungal necromass. The addition of high-quality litter led to higher total necromass and SOC in comparison to the addition of low-quality litter. Likely this difference depended on the higher availability of easily available C compounds in the Q. wutaishanica than in P. davidiana litters. The efficiency of SOC formation, determined by the percentage of SOC content gain divided by the litter C content loss, correlated with the microbial incorporation of P. davidiana litter-derived 13C into PLFAs and amino sugars. However, it increased sharply in the late phases of Q. wutaishanica litter decomposition despite the decreased 13C incorporation in PLFAs and amino sugars, suggesting the dominance of physical litter C stabilization. Compared to the high-quality litter, the low-quality litter induced lower but steadier necromass accumulation, thus increasing the SOC content in the long term. Litter quality, litter-derived 13C in PLFAs, and microbial CUE are the main drivers of litter-derived C use pathways. Our findings underpin the microbial C pump-regulated SOC formation, whereby differences in litter quality shape the composition of main microbial groups, leading to differences in enzyme activities and CUE, which determine necromass turnover and thus SOC formation.

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References

  • Aerts R (2006) The freezer defrosting: global warming and litter decomposition rates in cold biomes. J Ecol 94:713–724

    Article  Google Scholar 

  • Apostel C, Herschbach J, Bore EK, Spielvogel S, Kuzyakov Y, Dippold MA (2018) Food for microorganisms: position-specific 13C labeling and 13C-PLFA analysis reveals preferences for sorbed or necromass C. Geoderma 312:86–94

    Article  CAS  Google Scholar 

  • Bai XJ, Dippold MA, An SS (2021) Extracellular enzyme activity and stoichiometry as affected by soil microbial element limitation during leaf litter decomposition. Ecol Indic 121:107200

    Article  CAS  Google Scholar 

  • Bao SD (2000) Soil and agriculture chemistry analysis. China Agriculture Press, Beijing

    Google Scholar 

  • Bardgett RD, Saggar S (1994) Effects of heavy metal contamination on the short-term decomposition of labeled 14C glucose in a pasture soil. Soil Biol Biochem 26:727–733

    Article  CAS  Google Scholar 

  • Bonanomi G, De Filippis F, Cesarano G (2019) Linking bacterial and eukaryotic microbiota to litter chemistry: combining next generation sequencing with 13C CPMAS NMR spectroscopy. Soil Biol Biochem 129:110–121

    Article  CAS  Google Scholar 

  • Bradford MA, Berg B, Maynard DS (2016) Understanding the dominant controls on litter decomposition. J Ecol 104:229–238

    Article  CAS  Google Scholar 

  • Cai Y, Feng XJ (2023) Substrate and community regulations on microbial necromass accumulation from newly added and native soil carbon. Biol Fertil Soils 59:763–775

    Article  CAS  Google Scholar 

  • Castellano MJ, Mueller KE, Olk DC (2015) Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept. Glob Change Biol 21:3200–3209

    Article  Google Scholar 

  • Chen J, Jia B, Gang S, Li Y, Li F-C, Mou XM, Kuzyakov Y, Li XG (2022) Decoupling of soil organic carbon and nutrient mineralization across plant communities as affected by microbial stoichiometry. Biol Fertil Soils 58:693–706

    Article  CAS  Google Scholar 

  • Cotrufo MF, Soong JL, Horton AJ (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci 8:776–779

    Article  CAS  Google Scholar 

  • Craig ME, Geyer KM, Beidler KV (2022) Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits. Nat Commun 13:1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui J, Zhu Z, Xu X (2020) Carbon and nitrogen recycling from microbial necromass to cope with C: N stoichiometric imbalance by priming. Soil Biol Biochem 142:107720

    Article  CAS  Google Scholar 

  • Deng F, Liang C (2021) Revisiting the quantitative contribution of microbial necromass to soil carbon pool: stoichiometric control by microbes and soil. Soil Biol Biochem 165:108486

    Article  Google Scholar 

  • Dippold MA, Boesel S, Gunina A, Kuzyakov Y, Glaser B (2014) Improved δ13C analysis of amino sugars in soil by ion chromatography-oxidation-isotope ratio mass spectrometry. Rapid Commun Mass SP 28:569–576

    Article  CAS  Google Scholar 

  • Domeignoz-Horta LA, Shinfuku M, Junier P (2021) Direct evidence for the role of microbial community composition in the formation of soil organic matter composition and persistence. ISME Commun 1:64

    Article  PubMed  PubMed Central  Google Scholar 

  • Don A, Böhme IH, Dohrmann AB, Poeplau C, Tebbe CC (2017) Microbial community composition affects soil organic carbon turn-over in mineral soils. Biol Fertil Soils 53:445–456

    Article  CAS  Google Scholar 

  • Fanina N, Alavoine G, Bertrand I (2020) Temporal dynamics of litter quality, soil properties and microbial strategies as main drivers of the priming effect. Geoderma 377:114576

    Article  Google Scholar 

  • Fulton-Smith S, Cotrufo MF (2019) Pathways of soil organic matter formation from above and belowground inputs in a Sorghum bicolor bioenergy crop. GCB Bioenergy 11:971–987

    Article  CAS  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Article  CAS  Google Scholar 

  • Glaser B (2005) Compound specific stable isotope (δ13C) analysis in soil science. J Plant Nutr Soil Sc 168:633–648

    Article  CAS  Google Scholar 

  • Glaser B, Gross S (2005) Compound specific δ13C analysis of individual amino sugars–a tool to quantify timing and amount of soil microbial residue stabilization. Rapid Commun Mass Sp 19:1409–1416

    Article  CAS  Google Scholar 

  • Goodfellow M, Williams ST (1983) Ecology of actinobacterias. Annu Rev Microbiol 37:189–216

    Article  CAS  PubMed  Google Scholar 

  • Gunina A, Dippold M, Glaser B, Kuzyakov Y (2017) Turnover of microbial groups and cell components in soil: 13C analysis of cellular biomarkers. Biogeosciences 14:271–283

    Article  CAS  Google Scholar 

  • Heijboer A, de Ruiter PC, Bodelier PLE, Kowalchuk GA (2018) Modulation of litter decomposition by the soil microbial food web under influence of land use change. Front Microbiol 9:2860

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang W, Yu W, Yi B, Raman E, Yang J, Hammel KE, Timokhin VI, Lu C, Howe A, Weintraub-Leff SR, Hall SJ (2023) Contrasting geochemical and fungal controls on decomposition of lignin and soil carbon at continental scale. Nat Commun 14:2227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IUSS Working Group WRB (2022) World reference base for soil resources. International soil classification system for naming soils and creating legends for soil maps (4th ed.). International Union of Soil Sciences (IUSS)

  • Joergensen RG (2018) Amino sugars as specific indices for fungal and bacterial residues in soil. Biol Fert Soils 54:559–568

    Article  CAS  Google Scholar 

  • Joergensen RG (2022) Phospholipid fatty acids in soil—drawbacks and future prospects. Biol Fertil Soils 58:1–6

    Article  CAS  Google Scholar 

  • Jones DL, Hill PW, Smith AR, Farrell M, Ge T, Banning NC, Murphy DV (2018) Role of substrate supply on microbial carbon use efficiency and its role in interpreting soil microbial community-level physiological profiles (CLPP). Soil Biol Biochem 123:1–6

    Article  CAS  Google Scholar 

  • Kallenbach CM, Frey SD, Grandy AS (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kravchenko A, Guber A, Razavi BS (2019) Microbial spatial footprint as a driver of soil carbon stabilization. Nat Commun 10:3121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Hill PW, Jones DL (2007) Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant Soil 290:293–305

    Article  CAS  Google Scholar 

  • Lavallee JM, Conant RT, Paul EA, Cotrufo MF (2018) Incorporation of shoot versus root-derived 13C and 15N into mineral-associated organic matter fractions: results of a soil slurry incubation with dual-labelled plant material. Biogeochemistry 137:379–393

    Article  CAS  Google Scholar 

  • Li H, Yang S, Semenov MV (2021) Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community. Glob Change Biol 27:2763–2779

    Article  CAS  Google Scholar 

  • Liang C, Balser TC (2008) Preferential sequestration of microbial carbon in subsoils of a glacial- landscape toposequence. Dane County, WI, USA. Geoderma 148:113–119

    Article  CAS  Google Scholar 

  • Liang C, Balser TC (2011) Microbial production of recalcitrant organic matter in global soils: Implications for productivity and climate policy. Nat Rev Microbiol 9:34–38

    Article  Google Scholar 

  • Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Amelung W, Lehmann J, Kästner M (2019) Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Change Biol 23:234–241

    Google Scholar 

  • Lyu M, Homyak PM, Xie JS, Penuelas J, Ryan MG, Xiong XL, Sardans J, Lin WS, Wang MH, Chen GH, Yang YS (2023) Litter quality controls tradeoffs in soil carbon decomposition and replenishment in a subtropical forest. J Ecol 1:1–13

    Google Scholar 

  • Maynard DS, Crowther TW, Bradford MA (2017) Fungal interactions reduce carbon use efficiency. Ecol Lett 20:1034–1042

    Article  PubMed  Google Scholar 

  • Nannipieri P (2020) Soil is still an unknown biological system. Appl Sci 10:3717

    Article  CAS  Google Scholar 

  • Nunan N, Leloup J, Ruamps LS, Pouteau V, Chenu C (2018) Effects of habitat constraints on soil microbial community function. Sci Rep 1:4057

    Article  Google Scholar 

  • Olagoke FK, Bettermann A, Nguyen PTB, Redmile-Gordon M, Babin D, Smalla K, Nesme J, Sorensen SJ, Kalbitz K, Vogel C (2022) Importance of substrate quality and clay content on microbial extracellular polymeric substances production and aggregate stability in soils. Biol Fertil Soils 58:435–457

    Article  CAS  Google Scholar 

  • Paul EA, Clark FE (1989) Soil microbiology and biochemistry. Academic Press, San Diego, CA

    Book  Google Scholar 

  • Pausch J, Kramer S, Scharroba A, Scheunemann N, Butenschoen O, Kandeler E (2016) Small but active–pool size does not matter for carbon incorporation in belowground food webs. Funct Ecol 30:479–489

    Article  Google Scholar 

  • Peixoto L, Elsgaard L, Rasmussen J (2020) Decreased rhizodeposition, but increased microbial carbon stabilization with soil depth down to 3.6 m. Soil Biol Biochem 150:108008

    Article  CAS  Google Scholar 

  • Pereira S, Burešová A, Kopecky J (2019) Litter traits and rainfall reduction alter microbial litter decomposers: the evidence from three Mediterranean forests. FEMS Microbiol Ecol 95:168

    Article  Google Scholar 

  • Poirier V, Roumet C, Munson AD (2018) The root of the matter: linking root traits and soil organic matter stabilization processes. Soil Biol Biochem 120:246–259

    Article  CAS  Google Scholar 

  • Poll C, Ingwersen J, Stemmer M, Gerzabek MH, Kandeler E (2006) Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. Eur J Soil Sci 57:583–595

    Article  Google Scholar 

  • Rubino M, Dungait JAJ, Evershed RP, Bertolini T, De Angelis P, Donofrio A, Lagomarsino A, Lubritto C, Merola A, Terrasi F, Cotrufo MF (2010) Carbon input belowground is the major C flux contributing to leaf litter mass loss: Evidences from a 13C labelled-leaf litter experiment. Soil Biol Biochem 42:1009–1016

    Article  CAS  Google Scholar 

  • Sarquis A, Sierra CA (2023) Information content in time series of litter decomposition studies and the transit time of litter in arid lands. Biogeosciences 20:1759–1771

    Article  Google Scholar 

  • Sauvadet M, Lashermes G, Alavoine G, Recous S, Chauvat M, Maron PA, Bertrand I (2018) High carbon use efficiency and low priming effect promote soil C stabilization under reduced tillage. Soil Biol Biochem 123:64–73

    Article  CAS  Google Scholar 

  • Shahbaz M, Kuzyakov Y, Sanaullah M, Heitkamp F, Zelenev V, Kumar A, Blagodatskaya E (2017) Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: mechanisms and thresholds. Biol Fertil Soils 53:287–301

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Shah JF, Findlay SG, Kuehn KA, Moorhead DL (2015) Scaling microbial biomass, metabolism and resource supply. Biogeochemistry 122:175–190

    Article  Google Scholar 

  • Sokol NW, Sanderman J, Bradford MA (2019) Pathways of mineral-associated soil organic matter formation: integrating the role of plant carbon source, chemistry, and point of entry. Glob Change Biol 25:12–24

    Article  Google Scholar 

  • Sokol NW, Slessarev E, Marschmann GL (2022) Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nat Rev Microbiol 20:415–430

    Article  CAS  PubMed  Google Scholar 

  • Tao F, Huang Y, Hungate BA (2023) Microbial carbon use efficiency promotes global soil carbon storage. Nature 618:981–985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trivedi P, Delgado-Baquerizo M, Trivedi C (2016) Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships. ISME J 10:2593–2604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vesterdal L, Schmidt IK, Callesen I, Nilsson LO, Gundersen P (2008) Carbon and nitrogen in forest floor and mineral soil under six common European tree species. Forest Ecol Manag 255:35–48

    Article  Google Scholar 

  • Wang Q, Wang S, He T, Liu L, Wu J (2014) Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biol Biochem 71:13–20

    Article  CAS  Google Scholar 

  • Wang C, Qu L, Yang L, Liu D, Bai E (2021) Large-scale importance of microbial carbon use efficiency and necromass to soil organic carbon. Glob Change Biol 27:2039–2048

    Article  CAS  Google Scholar 

  • Wang BR, An SS, Liang C, Liu Y, Kuzyakov Y (2022) Microbial necromass as the source of soil organic carbon in global ecosystems. Soil Biol Biochem 162:108422

    Article  Google Scholar 

  • Zhang XD, Amelung W (1996) Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol Biochem 28:1201–1206

    Article  CAS  Google Scholar 

  • Zheng TT, Miltner A, Liang C, Nowak KM, Kastner M (2023) Turnover of bacterial biomass to soil organic matter via fungal biomass and its metabolic implications. Soil Biol Biochem 180:108995

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (42307442, 42077072), China Postdoctoral Science Foundation (2022M720987), Natural Science Foundation of Hebei Province of Youth (C2022205030), Advanced Programs of Hebei Province Postdoctoral Research Project (B2023003026), and Science Foundation of Hebei Normal University (L2022B36). Michaela A. Dippold conducted this study in close interaction with further studies in the framework of the priority program 2322 “Soil Systems–System ecology of soils” funded by the DFG, project number DFG DI 2136/17-1.

Funding

National Natural Science Foundation of China, 42307442, Xuejuan Bai, 42077072, Xuejuan Bai, Postdoctoral Research Foundation of China, 2022M720987, Xuejuan Bai, Science Research Project of Hebei Education Department (BJK2024199), Natural Science Foundation of Hebei Province, C2022205030, Xuejuan Bai, Advanced Programs of Hebei Province Postdoctoral Research Project, B2023003026, Xuejuan Bai, Science Foundation of Hebei Normal University, L2022B36, Xuejuan Bai.

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All authors contributed to research. The manuscript was primarily written by Xuejuan Bai, Guoqing Zhai, and Michaela Dippold, with contributions from Shaoshan An and Jingze Liu. The data were analyzed by Baorong Wang. Zhijing Xue edited the language. All authors have several times revised the manuscript and given approval to the final version of the manuscript.

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Correspondence to Shaoshan An or Jingze Liu.

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Bai, X., Zhai, G., Wang, B. et al. Litter quality controls the contribution of microbial carbon to main microbial groups and soil organic carbon during its decomposition. Biol Fertil Soils 60, 167–181 (2024). https://doi.org/10.1007/s00374-023-01792-8

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