Improved model simulation of soil carbon cycling by representing the microbially derived organic carbon pool

Hiederer R, Köchy M. Global soil organic carbon estimates and the harmonized world soil database. EUR. 2011;79:25225.

Google Scholar 

Scharlemann JPW, Tanner EVJ, Hiederer R, Kapos V. Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Manag. 2014;5:81–91.

CAS  Article  Google Scholar 

Wieder WR, Bonan GB, Allison SD. Global soil carbon projections are improved by modelling microbial processes. Nat Clim Chang. 2013;3:909–12.

CAS  Article  Google Scholar 

Schimel JP, Weintraub MN. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem. 2003;35:549–63.

CAS  Article  Google Scholar 

Huang Y, Guenet B, Ciais P, Janssens IA, Soong JL, Wang Y, et al. ORCHIMIC (v1.0), a microbe-mediated model for soil organic matter decomposition. Geosci Model Dev. 2018;11:2111–38.

CAS  Article  Google Scholar 

Georgiou K, Abramoff RZ, Harte J, Riley WJ, Torn MS. Microbial community-level regulation explains soil carbon responses to long-term litter manipulations. Nat Commun. 2017;8:1223.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Kelleher BP, Simpson AJ. Humic substances in soils: are they really chemically distinct? Environ Sci Technol. 2006;40:4605–11.

CAS  PubMed  Article  Google Scholar 

Wang C, Wang X, Pei G, Xia Z, Peng B, Sun L, et al. Stabilization of microbial residues in soil organic matter after two years of decomposition. Soil Biol Biochem. 2020;141:107687.

CAS  Article  Google Scholar 

Cotrufo MF, Wallenstein M, Boot C, Denef K, Paul E. 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 Change Biol. 2013;19:988–95.

Article  Google Scholar 

Zhu X, Jackson RD, DeLucia EH, Tiedje JM, Liang C. The soil microbial carbon pump: from conceptual insights to empirical assessments. Glob Change Biol. 2020;26:6032–9.

Article  Google Scholar 

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

CAS  Article  Google Scholar 

Torn MS, Trumbore SE, Chadwick OA, Vitousek PM, Hendricks DM. Mineral control of soil organic carbon storage and turnover. Nature. 1997;389:170–3.

CAS  Article  Google Scholar 

Dwivedi D, Riley WJ, Torn MS, Spycher N, Maggi F, Tang JY. Mineral properties, microbes, transport, and plant-input profiles control vertical distribution and age of soil carbon stocks. Soil Biol Biochem. 2017;107:244–59.

CAS  Article  Google Scholar 

Mikutta R, Kleber M, Torn MS, Jahn R. Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry. 2006;77:25–56.

CAS  Article  Google Scholar 

Liang C, Balser TC. Microbial production of recalcitrant organic matter in global soils: Implications for productivity and climate policy. Nat Rev Microbiol. 2011;9:75–75.

CAS  PubMed  Article  Google Scholar 

Khan KS, Mack R, Castillo X, Kaiser M, Joergensen RG. Microbial biomass, fungal and bacterial residues, and their relationships to the soil organic matter C/N/P/S ratios. Geoderma. 2016;271:115–23.

CAS  Article  Google Scholar 

Liang C, Amelung W, Lehmann J, Kästner M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol. 2019;25:3578–90.

PubMed  Article  Google Scholar 

Kögel-Knabner I. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter: fourteen years on. Soil Biol Biochem. 2017;105:A3–8.

Article  CAS  Google Scholar 

Todd-Brown KEO, Randerson JT, Post WM, Hoffman FM, Tarnocai C, Schuur EAG, et al. Causes of variation in soil carbon simulations from CMIP5 Earth System Models and comparison with observations. Biogeosciences. 2013;10:1717–36.

Article  Google Scholar 

Parton WJ, Schimel DS, Cole CV, Ojima DS. Analysis of factors controlling soil organic matter levels in great plains grasslands. Soil Sci Soc Am J. 1987;51:1173–9.

CAS  Article  Google Scholar 

Wang G, Post WM, Mayes MA. Development of microbial‐enzyme‐mediated decomposition model parameters through steady‐state and dynamic analyses. Ecol Appl. 2013;23:255–72.

PubMed  Article  Google Scholar 

Wang G, Mayes MA, Gu L, Schadt CW. Representation of dormant and active microbial dynamics for ecosystem modeling. PLoS ONE. 2014;9:e89252.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Wang G, Jagadamma S, Mayes MA, Schadt CW, Steinweg JM, Gu L, et al. Microbial dormancy improves development and experimental validation of ecosystem model. ISME J. 2015;9:226–37.

CAS  PubMed  Article  Google Scholar 

German D, Marcelo K, Stone M, Allison S. The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob Change Biol. 2012;18:1468–79.

Article  Google Scholar 

Allison SD, Wallenstein MD, Bradford MA. Soil-carbon response to warming dependent on microbial physiology. Nat Geosci. 2010;3:336–40.

CAS  Article  Google Scholar 

Li J, Wang G, Allison SD, Mayes MA, Luo Y. Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity. Biogeochemistry. 2014;119:67–84.

Article  Google Scholar 

Wieder WR, Grandy AS, Kallenbach CM, Bonan GB. Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model. Biogeosciences. 2014;11:3899–917.

Article  CAS  Google Scholar 

Tang J, Riley WJ. Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Chang. 2015;5:56–60.

CAS  Article  Google Scholar 

Sulman BN, Moore JA, Abramoff R, Averill C, Kivlin S, Georgiou K, et al. Multiple models and experiments underscore large uncertainty in soil carbon dynamics. Biogeochemistry. 2018;141:109–23.

CAS  Article  Google Scholar 

Sulman BN, Phillips RP, Oishi AC, Shevliakova E, Pacala SW. Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO₂. Nat Clim Change. 2014;4:1099–102.

CAS  Article  Google Scholar 

Lawrence C, Neff J, Schimel J. Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment. Soil Biol Biochem. 2009;41:1923–34.

CAS  Article  Google Scholar 

Wang X, Wang C, Cotrufo MF, Sun L, Jiang P, Liu Z, et al. Elevated temperature increases the accumulation of microbial necromass nitrogen in soil via increasing microbial turnover. Glob Change Biol. 2020;26:5277–89.

Article  Google Scholar 

Throckmorton HM, Bird JA, Dane L, Firestone MK, Horwath WR. The source of microbial C has little impact on soil organic matter stabilisation in forest ecosystems. Ecol Lett. 2012;15:1257–65.

PubMed  Article  Google Scholar 

Kindler R, Miltner A, Richnow H-H, Kästner M. Fate of gram-negative bacterial biomass in soil—mineralization and contribution to SOM. Soil Biol Biochem. 2006;38:2860–70.

CAS  Article  Google Scholar 

Schweigert M, Herrmann S, Miltner A, Fester T, Kästner M. Fate of ectomycorrhizal fungal biomass in a soil bioreactor system and its contribution to soil organic matter formation. Soil Biol Biochem. 2015;88:120–7.

CAS  Article  Google Scholar 

Derrien D, Amelung W. Computing the mean residence time of soil carbon fractions using stable isotopes: impacts of the model framework. Eur J Soil Sci. 2011;62:237–52.

Article  Google Scholar 

Dormand JR, Prince PJ. A family of embedded Runge-Kutta formulae. J Comput Appl Math. 1980;6:19–26.

Article  Google Scholar 

Shampine LF, Reichelt MW. The MATLAB ODE suite. Siam J Sci Comput. 1997;18:1–22.

Article  Google Scholar 

Coleman TF, Li Y. On the convergence of reflective newton methods for large-scale nonlinear minimization subject to bounds. Math Program. 1994;67:189–224.

Article  Google Scholar 

Coleman TF, Li Y. An interior trust region approach for nonlinear minimization subject to bounds. SIAM J Optim. 1996;6:418–45.

Article  Google Scholar 

Moré JJ. The Levenberg–Marquardt algorithm: implementation and theory. In: Watson GA (ed). Numerical Analysis. Springer: Berlin, Heidelberg, 1978, p. 105–16.

Leave-one-out cross-validation. In: Sammut C, Webb GI, editors. Encyclopedia of machine learning. Boston, MA: Springer USA; 2010. p. 600–1.

Wang C, Qu L, Yang L, Liu D, Morrissey E, Miao R, et al. Large-scale importance of microbial carbon use efficiency and necromass to soil organic carbon. Glob Chang Biol. 2021.

Farrell M, Prendergast-Miller M, Jones DL, Hill PW, Condron LM. Soil microbial organic nitrogen uptake is regulated by carbon availability. Soil Biol Biochem. 2014;77:261–7.

CAS  Article  Google Scholar 

Hagerty SB, Allison SD, Schimel JP. Evaluating soil microbial carbon use efficiency explicitly as a function of cellular processes: implications for measurements and models. Biogeochemistry. 2018;140:269–83.

CAS  Article  Google Scholar 

Qiao Y, Wang J, Liang G, Du Z, Zhou J, Zhu C, et al. Global variation of soil microbial carbon-use efficiency in relation to growth temperature and substrate supply. Sci Rep. 2019;9:5621.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Krinner G, Viovy N, de Noblet-Ducoudré N, Ogée J, Polcher J, Friedlingstein P, et al. A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system. Glob Biogeochem Cycles. 2005;19:GB1015.

Article  CAS  Google Scholar 

Wang G, Post WM, Mayes MA, Frerichs JT, Sindhu J. Parameter estimation for models of ligninolytic and cellulolytic enzyme kinetics. Soil Biol Biochem. 2012;48:28–38.

Article  CAS  Google Scholar 

Davidson EA, Janssens IA. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature. 2006;440:165–73.

CAS  PubMed  Article  Google Scholar 

Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol. 2017;37:4302–15.

Article  Google Scholar 

Guevara M, Taufer M, Vargas R. Gap-free global annual soil moisture: 15 km grids for 1991–2018. Earth Syst Sci Data. 2020;2020:1–65.

Google Scholar 

Kalnay E, Kanamitsu M, Kistler R, Collins W, Deaven D, Gandin L, et al. The NCEP/NCAR 40-year reanalysis project. Bull Am Meteorol Soc. 1996;77:437–72.

Article  Google Scholar 

Batjes NH. Harmonized soil property values for broad-scale modelling (WISE30sec) with estimates of global soil carbon stocks. Geoderma. 2016;269:61–8.

CAS  Article  Google Scholar 

Hengl T, Mendes de Jesus J, Heuvelink GBM, Ruiperez Gonzalez M, Kilibarda M, Blagotić A, et al. SoilGrids250m: global gridded soil information based on machine learning. PLoS ONE. 2017;12:e0169748.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Olson DM, Dinerstein E. The Global 200: a representation approach to conserving the earth’s most biologically valuable ecoregions. Conserv Biol. 1998;12:502–15.

Article  Google Scholar 

Kögel-Knabner I. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem. 2002;34:139–62.

Article  Google Scholar 

Fernandez CW, Koide RT. Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biol Biochem. 2014;77:150–7.

CAS  Article  Google Scholar 

Hemkemeyer M, Dohrmann AB, Christensen BT, Tebbe CC. Bacterial preferences for specific soil particle size fractions revealed by community analyses. Front Microbiol. 2018;9:149.

PubMed  PubMed Central  Article  Google Scholar 

Mills A. Keeping in touch: microbial life on soil particle surfaces. Adv Agron. 2003;78:1–43.

Article  Google Scholar 

Kindler R, Miltner A, Thullner M, Richnow H-H, Kästner M. Fate of bacterial biomass derived fatty acids in soil and their contribution to soil organic matter. Org Geochem. 2009;40:29–37.

CAS  Article  Google Scholar 

Huang Y, Liang C, Duan X, Chen H, Li D. Variation of microbial residue contribution to soil organic carbon sequestration following land use change in a subtropical karst region. Geoderma. 2019;353:340–6.

CAS  Article  Google Scholar 

Ahrens B, Braakhekke MC, Guggenberger G, Schrumpf M, Reichstein M. Contribution of sorption, DOC transport and microbial interactions to the 14C age of a soil organic carbon profile: insights from a calibrated process model. Soil Biol Biochem. 2015;88:390–402.

CAS  Article  Google Scholar 

Nguyen RT, Harvey HR. Preservation via macromolecular associations during Botryococcus braunii decay: proteins in the Pula Kerogen. Org Geochem. 2003;34:1391–403.

CAS  Article  Google Scholar 

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

CAS  PubMed  PubMed Central  Article  Google Scholar 

Puget P, Angers DA, Chenu C. Nature of carbohydrates associated with water-stable aggregates of two cultivated soils. Soil Biol Biochem. 1998;31:55–63.

Article  Google Scholar 

Schmidt MWI, 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.

CAS  PubMed  Article  Google Scholar 

Spence A, Simpson AJ, McNally DJ, Moran BW, McCaul MV, Hart K, et al. The degradation characteristics of microbial biomass in soil. Geochim Cosmochim Acta. 2011;75:2571–81.

CAS  Article  Google Scholar 

Drigo B, Anderson IC, Kannangara GSK, Cairney JWG, Johnson D. Rapid incorporation of carbon from ectomycorrhizal mycelial necromass into soil fungal communities. Soil Biol Biochem. 2012;49:4–10.

CAS  Article  Google Scholar 

Wang G, Chen S. A review on parameterization and uncertainty in modeling greenhouse gas emissions from soil. Geoderma. 2012;170:206–16.

CAS  Article  Google Scholar 

Blagodatskaya Е, Blagodatsky S, Khomyakov N, Myachina O, Kuzyakov Y. Temperature sensitivity and enzymatic mechanisms of soil organic matter decomposition along an altitudinal gradient on Mount Kilimanjaro. Sci Rep. 2016;6:22240.

CAS  Article  Google Scholar 

German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem. 2011;43:1387–97.

CAS  Article  Google Scholar 

Wu J, Xiao H. Measuring the gross turnover time of soil microbial biomass C under incubation. Acta Pedol Sin. 2004;41:401–7.

CAS  Google Scholar 

Cheng W. Rhizosphere priming effect: Its functional relationships with microbial turnover, evapotranspiration, and C–N budgets. Soil Biol Biochem. 2009;41:1795–801.

CAS  Article  Google Scholar 

Luo Z, Tang Z, Guo X, Jiang J, Sun OJ. Non-monotonic and distinct temperature responses of respiration of soil microbial functional groups. Soil Biol Biochem. 2020;148:107902.

CAS  Article  Google Scholar 

de Graaff M-A, Classen AT, Castro HF, Schadt CW. Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol. 2010;188:1055–64.

PubMed  Article  CAS  Google Scholar 

Paul EA. The nature and dynamics of soil organic matter: plant inputs, microbial transformations, and organic matter stabilization. Soil Biol Biochem. 2016;98:109–26.

CAS  Article  Google Scholar 

Crowther TW, Sokol NW, Oldfield EE, Maynard DS, Thomas SM, Bradford MA. Environmental stress response limits microbial necromass contributions to soil organic carbon. Soil Biol Biochem. 2015;85:153–61.

CAS  Article  Google Scholar 

Ding X, Chen S, Zhang B, He H, Filley TR, Horwath WR. Warming yields distinct accumulation patterns of microbial residues in dry and wet alpine grasslands on the Qinghai-Tibetan Plateau. Biol Fertil Soils. 2020;56:881–92.

CAS  Article  Google Scholar 

Mao D, Luo L, Wang Z, Zhang C, Ren C. Variations in net primary productivity and its relationships with warming climate in the permafrost zone of the Tibetan Plateau. J Geogr Sci. 2015;25:967–77.

Article  Google Scholar 

Wu J, Feng Y, Zhang X, Wurst S, Tietjen B, Tarolli P, et al. Grazing exclusion by fencing non-linearly restored the degraded alpine grasslands on the Tibetan Plateau. Sci Rep. 2017;7:15202.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Li J, Wang G, Mayes MA, Allison SD, Frey SD, Shi Z, et al. Reduced carbon use efficiency and increased microbial turnover with soil warming. Glob Change Biol. 2019;25:900–10.

Article  Google Scholar 

Chen G, Ma S, Tian D, Xiao W, Jiang L, Xing A, et al. Patterns and determinants of soil microbial residues from tropical to boreal forests. Soil Biol Biochem. 2020;151:108059.

CAS  Article  Google Scholar 

Wang YP, Chen BC, Wieder WR, Leite M, Medlyn BE, Rasmussen M, et al. Oscillatory behavior of two nonlinear microbial models of soil carbon decomposition. Biogeosciences. 2014;11:1817–31.

CAS  Article  Google Scholar 

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

CAS  Article  Google Scholar 

Liang C, Cheng G, Wixon DL, Balser TC. An Absorbing Markov Chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry. 2011;106:303–9.

Article  Google Scholar 

Fan Z, Liang C. Significance of microbial asynchronous anabolism to soil carbon dynamics driven by litter inputs. Sci Rep. 2015;5:9575.

CAS  PubMed  PubMed Central  Article  Google Scholar