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Substrate and community regulations on microbial necromass accumulation from newly added and native soil carbon

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Abstract

Microbial necromass accrual via anabolism is an important process contributing to the formation and accumulation of stable soil organic C (SOC). Both substrates and microbial community traits impact the rate and efficiency of microbial biomass production, yet their effects on necromass accumulation patterns and efficiency remain unclear. Here we selected six substrates to investigate substrate and community regulations on microbial necromass accumulation over a 476-day model soil incubation including three stages (microbial growth–starvation–reactivation) with varied supply of substrates or 13C-labeled glucose. Microbial respiration, the composition of main microbial groups, and necromass (amino sugars) production were examined along with 13C analysis to compare necromass accumulation from new OC and native SOC. We found that relative to fast-decomposing substrates, slow-decomposing substrate like lignin induced slow but steady necromass accrual in a long term. Exogenous glucose input stimulated necromass accumulation from new and native SOC during reactivation, especially in C (or energy)-limited model soils. Furthermore, the accumulation efficiency of amino sugars sourced from SOC and 13C-labeled glucose were positively related, suggesting microbial communities and soil properties affect necromass accrual efficiency. However, there was quite some scatter in the correlation, suggesting potential substrate effect and uncertainty in this relationship. Hence, the efficiency of soil “microbial C pump” (i.e., microbial transformation of exogenous substrates into microbial byproducts) fueled by exogenous substrate and native SOC needs to be further investigated. Collectively, these findings provide new information on the dynamics and efficiency of microbial necromass accumulation from different substrates in soils.

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Data availability

The data that support the findings of this study are available on request from the corresponding author.

References

  • Adingo S, Yu J-R, Xuelu L, Li X, Jing S, Xiaong Z (2021) Variation of soil microbial carbon use efficiency (CUE) and its influence mechanism in the context of global environmental change: a review. PeerJ 9:e12131

    Article  PubMed  PubMed Central  Google Scholar 

  • Allison SD (2014) Modeling adaptation of carbon use efficiency in microbial communities. Front Microbiol 5:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Appuhn A, Joergensen RG (2006) Microbial colonisation of roots as a function of plant species. Soil Biol Biochem 38:1040–1051

    Article  CAS  Google Scholar 

  • Bååth E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963

    Article  Google Scholar 

  • Bai Z, Bodé S, Huygens D, Zhang X, Boeckx P (2013) Kinetics of amino sugar formation from organic residues of different quality. Soil Biol Biochem 57:814–821

    Article  CAS  Google Scholar 

  • Bailey VL, Peacock AD, Smith JL HB Jr (2002) Relationships between soil microbial biomass determined by chloroform fumigation–extraction, substrate-induced respiration, and phospholipid fatty acid analysis. Soil Biol Biochem 34:1385–1389

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Brown RW, Chadwick DR, Bending GD, Collins CD, Whelton HL, Daulton E, Covington JA, Bull ID, Jones DL (2022) Nutrient (C, N and P) enrichment induces significant changes in the soil metabolite profile and microbial carbon partitioning. Soil Biol Biochem 172:108779

    Article  CAS  Google Scholar 

  • Buckeridge KM, Mason KE, Ostle N, McNamara NP, Grant HK, Whitaker J (2022) Microbial necromass carbon and nitrogen persistence are decoupled in agricultural grassland soils. Commun Earth Environ 3:114

    Article  Google Scholar 

  • Cai Y, Ma T, Wang Y, Jia J, Jia Y, Liang C, Feng X (2022) Assessing the accumulation efficiency of various microbial carbon components in soils of different minerals. Geoderma 407:115562

    Article  CAS  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 

  • Chen Y, Neilson JW, Kushwaha P, Maier RM, Barberan A (2021) Life-history strategies of soil microbial communities in an arid ecosystem. ISME J 15:649–657

    Article  CAS  PubMed  Google Scholar 

  • Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995

    Article  PubMed  Google Scholar 

  • Craig ME, Geyer KM, Beidler KV, Brzostek ER, Frey SD, Stuart Grandy A, Liang C, Phillips RP (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, Liu S, Jones DL, Kuzyakov Y, Shibistova O, Wu J, Ge T (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 

  • Dendooven L, Alcántara-Hernández RJ, Valenzuela-Encinas C, Luna-Guido M, Perez-Guevara F, Marsch R (2010) Dynamics of carbon and nitrogen in an extreme alkaline saline soil: A review. Soil Biol Biochem 42:865–877

    Article  CAS  Google Scholar 

  • Deng S, Zheng X, Chen X, Zheng S, He X, Ge T, Kuzyakov Y, Wu J, Su Y, Hu Y (2021) Divergent mineralization of hydrophilic and hydrophobic organic substrates and their priming effect in soils depending on their preferential utilization by bacteria and fungi. Biol Fertil Soils 57:65–76

    Article  CAS  Google Scholar 

  • Ding GC, Pronk GJ, Babin D, Heuer H, Heister K, Kӧgel-Knabner I, Smalla K (2013) Mineral composition and charcoal determine the bacterial community structure in artificial soils. FEMS Microbiol Ecol 86:15–25

    Article  CAS  PubMed  Google Scholar 

  • Engelking B, Flessa H, Joergensen RG (2007) Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol Biochem 39:2111–2118

    Article  CAS  Google Scholar 

  • Feng X, Simpson MJ (2009) Temperature and substrate controls on microbial phospholipid fatty acid composition during incubation of grassland soils contrasting in organic matter quality. Soil Biol Biochem 41:804–812

    Article  CAS  Google Scholar 

  • Forster JC (1995) Soil sampling, handling, storage and analysis. In: Alef K, Nannapieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press Inc, San Diego, pp 49–121

    Chapter  Google Scholar 

  • Glaser B, Turrión M-B, Alef K (2004) Amino sugars and muramic acid-biomarkers for soil microbial community structure analysis. Soil Biol Biochem 36:399–407

    Article  CAS  Google Scholar 

  • Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 31:147–158

    Article  CAS  Google Scholar 

  • Guerrant GO, Moss CW (1984) Determination of monosaccharides as aldononitrile, O-methyloxime, alditol, and cyclitol acetate derivatives by gas chromatography. Anal Chem 56:633–638

    Article  CAS  Google Scholar 

  • Gunina A, Dippold MA, Glaser B, Kuzyakov Y (2014) Fate of low molecular weight organic substances in an arable soil: from microbial uptake to utilisation and stabilisation. Soil Biol Biochem 77:304–313

    Article  CAS  Google Scholar 

  • Gunina A, Kuzyakov Y (2022) From energy to (soil organic) matter. Glob Chang Biol 28:2169–2182

    Article  CAS  PubMed  Google Scholar 

  • Harris DJ, Horwath WR, Van Kessel C (2001) Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Sci Soc Am J 65:1853–1856

    Article  CAS  Google Scholar 

  • Hill PW, Farrar JF, Jones DL (2008) Decoupling of microbial glucose uptake and mineralization in soil. Soil Biol Biochem 40:616–624

    Article  CAS  Google Scholar 

  • Huang X, Liu S, Wang H, Hu Z, Li Z, You Y (2014) Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus urophylla in subtropical China. Soil Biol Biochem 73:42–48

    Article  CAS  Google Scholar 

  • Islam KR, Weil RR, Mulchi CL, Glenn SD (1997) Freeze-dried soil extraction method for the measurement of microbial biomass C. Biol Fertil Soils 24:205–210

    Article  CAS  Google Scholar 

  • Jagadamma S, Mayes MA, Phillips JR (2012) Selective sorption of dissolved organic carbon compounds by temperate soils. PLoS One 7:e50434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia J, Feng X, He J-S, He H, Lin L, Liu Z (2017) Comparing microbial carbon sequestration and priming in the subsoil versus topsoil of a Qinghai-Tibetan alpine grassland. Soil Biol Biochem 104:141–151

    Article  CAS  Google Scholar 

  • Joergensen RG (2018) Amino sugars as specific indices for fungal and bacterial residues in soil. Biol Fertil 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 

  • Kästner M, Miltner A, Thiele-Bruhn S, Liang C (2021) Microbial necromass in soils—linking microbes to soil processes and carbon turnover. Front Environ Sci 9:756378

    Article  Google Scholar 

  • Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems - a review. Plant Soil 256:41–66

    Article  CAS  Google Scholar 

  • LaRowe DE, Van Cappellen P (2011) Degradation of natural organic matter: a thermodynamic analysis. Geochim Cosmochim Acta 75:2030–2042

    Article  CAS  Google Scholar 

  • Liang C, Amelung W, Lehmann J, Kastner M (2019) Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol 25:3578–3590

    Article  PubMed  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 

  • Liu X, Hou Y, Yu Z, Wang Y, Zhou S, Jiang B, Liao Y (2020) Comparison of molecular transformation of dissolved organic matter in vermicomposting and thermophilic composting by ESI-FT-ICR-MS. Environ Sci Pollut Res 27:43480–43492

    Article  CAS  Google Scholar 

  • Manzoni S, Čapek P, Porada P, Thurner M, Winterdahl M, Beer C, Brüchert V, Frouz J, Herrmann AM, Lindahl BD, Lyon SW, Šantrůčková H, Vico G, Way D (2018) Reviews and syntheses: carbon use efficiency from organisms to ecosystems - definitions, theories, and empirical evidence. Biogeosciences 15:5929–5949

    Article  CAS  Google Scholar 

  • Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91

    Article  CAS  PubMed  Google Scholar 

  • Martin JP, Haider K, Linhares LF (1979) Decomposition and stabilization of ring-14C-labeled catechol in soil. Soil Sci Soc Am J 43:100–104

    Article  CAS  Google Scholar 

  • Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

    Article  CAS  Google Scholar 

  • Miyamoto-Shinohara Y, Imaizumi T, Sukenobe J, Murakami Y, Kawamura S, Komatsu Y (2000) Survival rate of microbes after freeze-drying and long-term storage. Cryobiology 41:251–255

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, Nakahara T (2006) Survival curves for microbial species stored by freeze-drying. Cryobiology 52:27–32

    Article  PubMed  Google Scholar 

  • Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Olagoke FK, Bettermann A, Nguyen PTB, Redmile-Gordon M, Babin D, Smalla K, Nesme J, Sørensen 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 

  • Pinnataip R, Lee BP (2021) Oxidation chemistry of catechol utilized in designing stimuli-responsive adhesives and antipathogenic biomaterials. ACS Omega 6:5113–5118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing. R Development Core Team, Vienna

  • Rolfe MD, Rice CJ, Lucchini S, Pin C, Thompson A, Cameron AD, Alston M, Stringer MF, Betts RP, Baranyi J, Peck MW, Hinton JC (2012) Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. J Bacteriol 194:686–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939

    Article  PubMed  Google Scholar 

  • Soares M, Rousk J (2019) Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry. Soil Biol Biochem 131:195–205

    Article  CAS  Google Scholar 

  • Sokol NW, Bradford MA (2019) Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat Geosci 12:46–53

    Article  CAS  Google Scholar 

  • Wickland KP, Neff JC, Aiken GR (2007) Dissolved organic carbon in Alaskan boreal forest: sources, chemical characteristics, and biodegradability. Ecosystems 10:1323–1340

    Article  CAS  Google Scholar 

  • Wild B, Schnecker J, Alves RJ, Barsukov P, Barta J, Capek P, Gentsch N, Gittel A, Guggenberger G, Lashchinskiy N, Mikutta R, Rusalimova O, Santruckova H, Shibistova O, Urich T, Watzka M, Zrazhevskaya G, Richter A (2014) Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil. Soil Biol Biochem 75:143–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Schimel JP, Thornton PE, Song X, Yuan F, Goswami S (2014) Substrate and environmental controls on microbial assimilation of soil organic carbon: a framework for Earth system models. Ecol Lett 17:547–555

    Article  PubMed  Google Scholar 

  • Xu Y, Gao X, Liu Y, Li S, Liang C, Lal R, Wang J (2022) Differential accumulation patterns of microbial necromass induced by maize root vs. shoot residue addition in agricultural Alfisols. Soil Biol Biochem 164:108474

    Article  CAS  Google Scholar 

  • Xu Y, Seshadri B, Sarkar B, Wang H, Rumpel C, Sparks D, Farrell M, Hall T, Yang X, Bolan N (2018) Biochar modulates heavy metal toxicity and improves microbial carbon use efficiency in soil. Sci Total Environ 621:148–159

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, 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 

  • Zhou C, Liu Y, Liu C, Liu Y, Tfaily MM (2019) Compositional changes of dissolved organic carbon during its dynamic desorption from hyporheic zone sediments. Sci Total Environ 658:16–23

    Article  CAS  PubMed  Google Scholar 

  • Zhu E, Cao Z, Jia J, Liu C, Zhang Z, Wang H, Dai G, He JS, Feng X (2021) Inactive and inefficient: warming and drought effect on microbial carbon processing in alpine grassland at depth. Glob Chang Biol 27:2241–2253

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Plant Science Facility of the Institute of Botany, Chinese Academy of Sciences for bulk soil analysis.

Funding

This study was financially supported by the National Key R&D Program of China (2019YFA0607303), the National Natural Science Foundation of China (42103028), and the Chinese Academy of Sciences K. C. Wong Education Foundation (GJTD-2019-10).

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Authors and Affiliations

  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Yue Cai & Xiaojuan Feng

  2. China National Botanical Garden, Beijing, 100093, China

    Yue Cai & Xiaojuan Feng

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yue Cai & Xiaojuan Feng

  4. School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, 100083, China

    Yue Cai

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  1. Yue Cai
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Y. C. and X. F. conceived the idea and designed the study. Y. C. conducted the experiment and analyzed the data; Y. C. and X. F. wrote the manuscript.

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Correspondence to Xiaojuan Feng.

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Cai, Y., Feng, X. Substrate and community regulations on microbial necromass accumulation from newly added and native soil carbon. Biol Fertil Soils 59, 763–775 (2023). https://doi.org/10.1007/s00374-023-01745-1

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