Advertisement

Biogeochemistry

, Volume 137, Issue 1–2, pp 51–71 | Cite as

The Millennial model: in search of measurable pools and transformations for modeling soil carbon in the new century

  • Rose AbramoffEmail author
  • Xiaofeng Xu
  • Melannie Hartman
  • Sarah O’Brien
  • Wenting Feng
  • Eric Davidson
  • Adrien Finzi
  • Daryl Moorhead
  • Josh Schimel
  • Margaret Torn
  • Melanie A. Mayes
Synthesis and Emerging Ideas

Abstract

Soil organic carbon (SOC) can be defined by measurable chemical and physical pools, such as mineral-associated carbon, carbon physically entrapped in aggregates, dissolved carbon, and fragments of plant detritus. Yet, most soil models use conceptual rather than measurable SOC pools. What would the traditional pool-based soil model look like if it were built today, reflecting the latest understanding of biological, chemical, and physical transformations in soils? We propose a conceptual model—the Millennial model—that defines pools as measurable entities. First, we discuss relevant pool definitions conceptually and in terms of the measurements that can be used to quantify pool size, formation, and destabilization. Then, we develop a numerical model following the Millennial model conceptual framework to evaluate against the Century model, a widely-used standard for estimating SOC stocks across space and through time. The Millennial model predicts qualitatively similar changes in total SOC in response to single factor perturbations when compared to Century, but different responses to multiple factor perturbations. We review important conceptual and behavioral differences between the Millennial and Century modeling approaches, and the field and lab measurements needed to constrain parameter values. We propose the Millennial model as a simple but comprehensive framework to model SOC pools and guide measurements for further model development.

Keywords

Modeling Soil carbon Organic matter Microbial activity Decomposition Global change 

Notes

Acknowledgements

The Millennial model code, model inputs, and the model output used in this manuscript are archived at a GITHUB Repository (https://github.com/email-clm/Millennial) that is publicly accessible. The authors would like to thank the Carbon Cycle Interagency Working Group, via the US Carbon Cycle Science Program under the auspices of the US Global Change Research Program, for providing funding for the “Celebrating the 2015 International Decade of Soil – Understanding Soil’s Resilience and Vulnerability,” workshop held at the University Corporation for Atmospheric Research in Boulder, CO, USA on 14–16 March 2016. We would also like to thank the University Corporation for Atmospheric Research for providing meeting space, as well as the 36 workshop participants, William J. Riley, and three anonymous reviewers for helpful comments and discussion. Lawrence Berkeley National Laboratory is managed and operated by the Regents of the University of California under Contract DE-AC02-05CH11231 with the US Department of Energy. Argonne National Laboratory is managed by UChicago Argonne, LLC, under contract DE-AC02-06CH11357 with the US Department of Energy. Oak Ridge National Laboratory is managed by the University of Tennessee-Battelle, LLC, under Contract DE-AC05-00OR22725 with the US Department of Energy.

Compliance with ethical standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Abramoff RZ, Finzi AC (2016) Seasonality and partitioning of root allocation to rhizosphere soils in a midlatitude forest. Ecosphere.  https://doi.org/10.1002/ecs2.1547 Google Scholar
  2. Abramoff RZ, Davidson EA, Finzi AC (2017) A parsimonious modular approach to building a mechanistic belowground carbon and nitrogen model. J Geophys Res Biogeosci 122:2418–2434CrossRefGoogle Scholar
  3. Ahrens B, Braakhekke MC, Guggenberger G et al (2015) 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 88:390–402CrossRefGoogle Scholar
  4. Albalasmeh AA, Ghezzehei TA (2013) Interplay between soil drying and root exudation in rhizosheath development. Plant Soil 374:739–751CrossRefGoogle Scholar
  5. Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81:361–373CrossRefGoogle Scholar
  6. Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256CrossRefGoogle Scholar
  7. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340CrossRefGoogle Scholar
  8. Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221CrossRefGoogle Scholar
  9. Averill C (2014) Divergence in plant and microbial allocation strategies explains continental patterns in microbial allocation and biogeochemical fluxes. Ecol Lett.  https://doi.org/10.1111/ele.12324 Google Scholar
  10. Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963CrossRefGoogle Scholar
  11. Bailey VL, Bond-Lamberty B, DeAngelis K et al (2017) Soil carbon cycling proxies: understanding their critical role in predicting climate change feedbacks. Glob Change Biol 00:1–11Google Scholar
  12. Baker NR, Allison SD (2015) Ultraviolet photodegradation facilitates microbial litter decomposition in a Mediterranean climate. Ecology 96:1994–2003CrossRefGoogle Scholar
  13. Blankinship JC, Fonte SJ, Six J, Schimel JP (2016) Plant versus microbial controls on soil aggregate stability in a seasonally dry ecosystem. Geoderma 272:39–50CrossRefGoogle Scholar
  14. Boddy E, Hill P, Farrar J, Jones D (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835CrossRefGoogle Scholar
  15. Bonan GB, Hartman MD, Parton WJ, Wieder WR (2013) Evaluating litter decomposition in earth system models with long-term litterbag experiments: an example using the Community Land Model version 4 (CLM4). Glob Change Biol 19:957–974CrossRefGoogle Scholar
  16. Bradford MA, Wieder WR, Bonan GB et al (2016) Managing uncertainty in soil carbon feedbacks to climate change. Nat Clim Change 6:751–758CrossRefGoogle Scholar
  17. Burns RG, DeForest JL, Marxsen J et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  18. Cai A, Feng W, Zhang W, Xu M (2016) Climate, soil texture, and soil types affect the contributions of fine-fraction-stabilized carbon to total soil organic carbon in different land uses across China. J Environ Manag 172:2–9CrossRefGoogle Scholar
  19. Castro HF, Classen AT, Austin EE et al (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007CrossRefGoogle Scholar
  20. Chenu C, Plante AF (2006) Clay-sized organo-mineral complexes in a cultivation chronosequence: revisiting the concept of the “primary organo-mineral complex”. Eur J Soil Sci 57:596–607CrossRefGoogle Scholar
  21. Cotrufo MF, Wallenstein MD, Boot CM et al (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 Change Biol 19:988–995CrossRefGoogle Scholar
  22. Cotrufo MF, Soong JL, Horton AJ et al (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci 8:776–779CrossRefGoogle Scholar
  23. Crawford JW, Deacon L, Grinev D et al (2012) Microbial diversity affects self-organization of the soil–microbe system with consequences for function. J R Soc Interface 9:1302–1310CrossRefGoogle Scholar
  24. Davidson EA, Samanta S, Caramori SS, Savage K (2012) The Dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Glob Change Biol 18:371–384CrossRefGoogle Scholar
  25. De Gryze S, Six J, Merckx R (2006) Quantifying water–stable soil aggregate turnover and its implication for soil organic matter dynamics in a model study. Eur J Soil Sci 57:693–707CrossRefGoogle Scholar
  26. DeAngelis KM, Pold G, Topçuoğlu BD et al (2015) Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6:104CrossRefGoogle Scholar
  27. Del Grosso SJ, Parton WJ, Mosier AR et al (2005) Modeling soil CO2 emissions from ecosystems. Biogeochemistry 73:71–91CrossRefGoogle Scholar
  28. Denef K, Six J, Merckx R, Paustian K (2002) Short-term effects of biological and physical forces on aggregate formation in soils with different clay mineralogy. Plant Soil 246:185–200CrossRefGoogle Scholar
  29. Devêvre OC, Horwáth WR (2000) Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol Biochem 32:1773–1785CrossRefGoogle Scholar
  30. Dexter AR (1988) Advances in characterization of soil structure. Soil Tillage Res 11:199–238CrossRefGoogle Scholar
  31. Dwivedi D, Riley WJ, Torn MS, et al (2017) Mineral properties, microbes, transport, and plant-input profiles control vertical distribution and age of soil carbon stocks. Soil Biol Biochem 107:244–259CrossRefGoogle Scholar
  32. Ekschmitt K, Liu M, Vetter S et al (2005) Strategies used by soil biota to overcome soil organic matter stability—why is dead organic matter left over in the soil? Geoderma 128:167–176CrossRefGoogle Scholar
  33. Fahey TJ, Siccama TG, Driscoll CT et al (2005) The biogeochemistry of carbon at Hubbard Brook. Biogeochemistry 75:109–176CrossRefGoogle Scholar
  34. Feng W, Klaminder J, Boily J-F (2015) Thermal stability of goethite-bound natural organic matter is impacted by carbon loading. J Phys Chem A 119:12790–12796CrossRefGoogle Scholar
  35. Feng W, Shi Z, Jiang J et al (2016) Methodological uncertainty in estimating carbon turnover times of soil fractions. Soil Biol Biochem 100:118–124CrossRefGoogle Scholar
  36. Fontaine S, Barot S, Barré P et al (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280CrossRefGoogle Scholar
  37. Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Change 3:395–398CrossRefGoogle Scholar
  38. Georgiou K, Abramoff RZ, Harte J et al (2017) Microbial community-level regulation explains soil carbon responses to long-term litter manipulations. Nat Commun 8:1223CrossRefGoogle Scholar
  39. Gerke HH (2006) Preferential flow descriptions for structured soils. Z Pflanzenernähr Bodenkd 169:382–400CrossRefGoogle Scholar
  40. German DP, Marcelo KRB, Stone MM, Allison SD (2012) The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob Change Biol 18:1468–1479CrossRefGoogle Scholar
  41. Geyer KM, Kyker-Snowman E, Grandy AS, Frey SD (2016) Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127:173–188CrossRefGoogle Scholar
  42. Grant RF (2001) A review of Canadian ecosystem model—ecosys. In: Modeling carbon and nitrogen dynamics for soil management, p 173–264.  https://doi.org/10.1201/9781420032635.ch6
  43. Grant RF (2013) Modelling changes in nitrogen cycling to sustain increases in forest productivity under elevated atmospheric CO2 and contrasting site conditions. Biogeosciences 10:7703–7721CrossRefGoogle Scholar
  44. Hall SJ, McNicol G, Natake T, Silver WL (2015) Large fluxes and rapid turnover of mineral-associated carbon across topographic gradients in a humid tropical forest: insights from paired 14C analysis. Biogeosciences 12:2471–2487CrossRefGoogle Scholar
  45. Hanson PJ, Gill AL, Xu X et al (2016) Intermediate-scale community-level flux of CO2 and CH4 in a Minnesota peatland: putting the SPRUCE project in a global context. Biogeochemistry 129:255–272CrossRefGoogle Scholar
  46. Hararuk O, Obrist D, Luo Y (2013) Modelling the sensitivity of soil mercury storage to climate-induced changes in soil carbon pools. Biogeosciences 10:2393–2407CrossRefGoogle Scholar
  47. Heckman K, Throckmorton H, Clingensmith C et al (2014) Factors affecting the molecular structure and mean residence time of occluded organics in a lithosequence of soils under ponderosa pine. Soil Biol Biochem 77:1–11CrossRefGoogle Scholar
  48. Horn R, Taubner H, Wuttke M, Baumgartl T (1994) Soil physical properties related to soil structure. Soil Tillage Res 30:187–216CrossRefGoogle Scholar
  49. Jagadamma S, Mayes MA, Phillips JR (2012) Selective sorption of dissolved organic carbon compounds by temperate soils. PLoS ONE.  https://doi.org/10.1371/journal.pone.0050434 Google Scholar
  50. Jagadamma S, Megan Steinweg J, Mayes MA et al (2013) Decomposition of added and native organic carbon from physically separated fractions of diverse soils. Biol Fertil Soils 50:613–621CrossRefGoogle Scholar
  51. Jardine PM, McCarthy JF (1989) Mechanisms of dissolved organic carbon adsorption on soil.  https://doi.org/10.2136/sssaj1989.03615995005300050013x
  52. Jardine PM, Mayes MA, Mulholland PJ et al (2006) Vadose zone flow and transport of dissolved organic carbon at multiple scales in humid regimes. Vadose Zone J 5:140–152CrossRefGoogle Scholar
  53. Jastrow JD, Miller RM, Boutton TW (1996) Carbon dynamics of aggregate-associated organic matter estimated by carbon-13 natural abundance. Soil Sci Soc Am J 60:801CrossRefGoogle Scholar
  54. Jastrow JD, Miller RM, Lussenhop J (1998) Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 30:905–916CrossRefGoogle Scholar
  55. Jenkinson DS, Coleman K (2008) The turnover of organic carbon in subsoils. Part 2. Modelling carbon turnover. Eur J Soil Sci 59:400–413CrossRefGoogle Scholar
  56. Junicke H, Abbas B, Oentoro J et al (2014) Absolute quantification of individual biomass concentrations in a methanogenic coculture. AMB Express.  https://doi.org/10.1186/s13568-014-0035-x Google Scholar
  57. Kaiser K, Kalbitz K (2012) Cycling downwards—dissolved organic matter in soils. Soil Biol Biochem 52:29–32CrossRefGoogle Scholar
  58. Kaiser K, Guggenberger G, Zech W (1996) Sorption of DOM and DOM fractions to forest soils. Geoderma 74:281–303CrossRefGoogle Scholar
  59. Kalbitz K, Kaiser K (2008) Contribution of dissolved organic matter to carbon storage in forest mineral soils. Z Pflanzenernähr Bodenkd 171:52–60CrossRefGoogle Scholar
  60. Kallenbach CM, Frey SD, Grandy AS (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630CrossRefGoogle Scholar
  61. Kleber M, Sollins P, Sutton R (2007) A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85:9–24CrossRefGoogle Scholar
  62. Kleber M, Nico PS, Plante A et al (2011) Old and stable soil organic matter is not necessarily chemically recalcitrant: implications for modeling concepts and temperature sensitivity. Glob Change Biol 17:1097–1107CrossRefGoogle Scholar
  63. Kothawala DN, Moore TR, Hendershot WH (2009) Soil properties controlling the adsorption of dissolved organic carbon to mineral soils. Soil Sci Soc Am J 73:1831–1842CrossRefGoogle Scholar
  64. Koven CD, Riley WJ, Subin ZM et al (2013) The effect of vertically resolved soil biogeochemistry and alternate soil C and N models on C dynamics of CLM4. Biogeosciences 10:7109–7131CrossRefGoogle Scholar
  65. Lajtha K, Bowden RD, Nadelhoffer K (2014a) Twenty years of litter and root manipulations in a temperate deciduous forest: Insights into soil organic matter dynamics and stability. Soil Sci Soc Am J 78:261–269CrossRefGoogle Scholar
  66. Lajtha K, Townsend KL, Kramer MG et al (2014b) Changes to particulate versus mineral-associated soil carbon after 50 years of litter manipulation in forest and prairie experimental ecosystems. Biogeochemistry 119:341–360CrossRefGoogle Scholar
  67. Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68CrossRefGoogle Scholar
  68. Liao JD, Boutton TW, Jastrow JD (2006) Storage and dynamics of carbon and nitrogen in soil physical fractions following woody plant invasion of grassland. Soil Biol Biochem 38:3184–3196CrossRefGoogle Scholar
  69. Luo Y, Ahlström A, Allison SD et al (2015) Towards more realistic projections of soil carbon dynamics by earth system models. Glob Biogeochem Cycles.  https://doi.org/10.1002/2015gb005239 Google Scholar
  70. Manzoni S, Porporato A (2009) Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biol Biochem 41:1355–1379CrossRefGoogle Scholar
  71. Manzoni S, Schaeffer SM, Katul G et al (2014) A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biol Biochem 73:69–83CrossRefGoogle Scholar
  72. Marin-Spiotta E, Silver WL, Swanston CW, Ostertag R (2009) Soil organic matter dynamics during 80 years of reforestation of tropical pastures. Glob Change Biol 15:1584–1597CrossRefGoogle Scholar
  73. Martin JP, Martin WP, Page JB et al (1955) Soil aggregation. Adv Agron 7:1–37CrossRefGoogle Scholar
  74. Mayer LM (1994) Relationships between mineral surfaces and organic carbon concentrations in soils and sediments. Chem Geol 114:347–363CrossRefGoogle Scholar
  75. Mayes MA, Heal KR, Brandt CC et al (2012) Relation between soil order and sorption of dissolved organic carbon in temperate subsoils. Soil Sci Soc Am J 76:1027–1037CrossRefGoogle Scholar
  76. McCarthy JF, Ilavsky J, Jastrow JD et al (2008) Protection of organic carbon in soil microaggregates via restructuring of aggregate porosity and filling of pores with accumulating organic matter. Geochim Cosmochim Acta 72:4725–4744CrossRefGoogle Scholar
  77. Melillo JM, Butler S, Johnson J et al (2011) Soil warming, carbon–nitrogen interactions, and forest carbon budgets. Proc Natl Acad Sci USA 108:9508–9512CrossRefGoogle Scholar
  78. Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141CrossRefGoogle Scholar
  79. Norby RJ, Luo Y (2004) Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. N Phytol 162:281–293CrossRefGoogle Scholar
  80. O’Brien SL, Jastrow JD (2013) Physical and chemical protection in hierarchical soil aggregates regulates soil carbon and nitrogen recovery in restored perennial grasslands. Soil Biol Biochem 61:1–13CrossRefGoogle Scholar
  81. O’Brien SL, Jastrow JD, McFarlane KJ et al (2013) Decadal cycling within long-lived carbon pools revealed by dual isotopic analysis of mineral-associated soil organic matter. Biogeochemistry 112:111–125CrossRefGoogle Scholar
  82. Oleson KW, Lawrence DM, Bonan GB et al (2013) Technical description of version 4.5 of the Community Land Model (CLM). NCAR Tech. National Center for Atmospheric Research, BounderGoogle Scholar
  83. Parton WJ, Schimel DS, Cole CV et al (1987) Analysis of factors controlling soil organic matter levels in great plains grasslands. Soil Sci Soc Am J 51:1173–1179CrossRefGoogle Scholar
  84. Parton WJ, Scurlock JMO, Ojima DS et al (1995) Impact of climate change on grassland production and soil carbon worldwide. Glob Change Biol 1:13–22CrossRefGoogle Scholar
  85. Parton WJ, Hartman M, Ojima D, Schimel D (1998) DAYCENT and its land surface submodel: description and testing. Glob Planet Change 19:35–48CrossRefGoogle Scholar
  86. Parton WJ, Hanson PJ, Swanston C et al (2010) ForCent model development and testing using the Enriched Background Isotope Study experiment. J Geophys Res.  https://doi.org/10.1029/2009jg001193 Google Scholar
  87. Paustian K, Parton WJ, Persson J (1992) Modeling soil organic matter in organic-amended and nitrogen-fertilized long-term plots. Soil Sci Soc Am J 56:476–488CrossRefGoogle Scholar
  88. Plante AF, Conant RT, Paul EA et al (2006) Acid hydrolysis of easily dispersed and microaggregate-derived silt- and clay-sized fractions to isolate resistant soil organic matter. Eur J Soil Sci 57:456–467CrossRefGoogle Scholar
  89. Pronk GJ, Heister K, Ding G-C et al (2012) Development of biogeochemical interfaces in an artificial soil incubation experiment; aggregation and formation of organo-mineral associations. Geoderma 189–190:585–594CrossRefGoogle Scholar
  90. Ranjard L, Richaume A (2001) Quantitative and qualitative microscale distribution of bacteria in soil. Res Microbiol 152:707–716CrossRefGoogle Scholar
  91. Riley WJ, Maggi F, Kleber M et al (2014) Long residence times of rapidly decomposable soil organic matter: application of a multi-phase, multi-component, and vertically resolved model (BAMS1) to soil carbon dynamics. Geosci Model Dev 7:1335–1355CrossRefGoogle Scholar
  92. Rumpel C, Eusterhues K, Kögel-Knabner I (2010) Non-cellulosic neutral sugar contribution to mineral associated organic matter in top- and subsoil horizons of two acid forest soils. Soil Biol Biochem 42:379–382CrossRefGoogle Scholar
  93. Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Change Biol.  https://doi.org/10.1111/j.1365-2486.1995.tb00008.x Google Scholar
  94. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  95. Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56CrossRefGoogle Scholar
  96. Segoli M, De Gryze S, Dou F et al (2013) AggModel: a soil organic matter model with measurable pools for use in incubation studies. Ecol Model 263:1–9CrossRefGoogle Scholar
  97. Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651CrossRefGoogle Scholar
  98. Sierra CA, Trumbore SE, Davidson EA et al (2012) Predicting decadal trends and transient responses of radiocarbon storage and fluxes in a temperate forest soil.  https://doi.org/10.5194/bg-9-3013-2012
  99. Sierra CA, Trumbore SE, Davidson EA et al (2015) Sensitivity of decomposition rates of soil organic matter with respect to simultaneous changes in temperature and moisture. J Adv Model Earth Syst 7:335–356CrossRefGoogle Scholar
  100. Sinsabaugh RL, Shah JJF (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343CrossRefGoogle Scholar
  101. Sinsabaugh RL, Belnap J, Findlay SG et al (2014a) Extracellular enzyme kinetics scale with resource availability. Biogeochemistry 121:287–304CrossRefGoogle Scholar
  102. Sinsabaugh RL, Follstad Shah JJ, Findlay SG et al (2014b) Scaling microbial biomass, metabolism and resource supply. Biogeochemistry 122:175–190CrossRefGoogle Scholar
  103. Sinsabaugh RL, Moorhead DL, Xu X, Litvak ME (2017) Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production. N Phytol.  https://doi.org/10.1111/nph.14485 Google Scholar
  104. Sistla SA, Rastetter EB, Schimel JP (2014) Responses of a tundra system to warming using SCAMPS: a stoichiometrically coupled, acclimating microbe–plant–soil model. Ecol Monogr 84:151–170CrossRefGoogle Scholar
  105. Six J, Paustian K (2014) Aggregate-associated soil organic matter as an ecosystem property and a measurement tool. Soil Biol Biochem 68:A4–A9CrossRefGoogle Scholar
  106. Six J, Elliott ET, Paustian K, Doran JW (1998) Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62:1367–1377CrossRefGoogle Scholar
  107. Six J, Elliott ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103CrossRefGoogle Scholar
  108. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555CrossRefGoogle Scholar
  109. Smith AP, Bond-Lamberty B, Benscoter BW et al (2017) Shifts in pore connectivity from precipitation versus groundwater rewetting increases soil carbon loss after drought. Nat Commun.  https://doi.org/10.1038/s41467-017-01320-x Google Scholar
  110. Sollins P, Homann P, Caldwell BA (1996) Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74:65–105CrossRefGoogle Scholar
  111. Sollins P, Kramer MG, Swanston C et al (2009) Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–231CrossRefGoogle Scholar
  112. Steinweg JM, Plante AF, Conant RT et al (2008) Patterns of substrate utilization during long-term incubations at different temperatures. Soil Biol Biochem 40:2722–2728CrossRefGoogle Scholar
  113. Sulman BN, Phillips RP, Oishi AC et al (2014) Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO 2. Nat Clim Change 4:1099–1102CrossRefGoogle Scholar
  114. Suseela V, Conant RT, Wallenstein MD, Dukes JS (2012) Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Change Biol 18:336–348CrossRefGoogle Scholar
  115. Tang JY (2015) On the relationships between Michaelis–Menten kinetics, reverse Michaelis–Menten kinetics, Equilibrium Chemistry Approximation kinetics and quadratic kinetics. Geosci Model Dev Discuss 8:7663–7691CrossRefGoogle Scholar
  116. Tang J, Riley WJ (2015) Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Change.  https://doi.org/10.1038/nclimate2438 Google Scholar
  117. Thornton PE, Lamarque J-F, Rosenbloom NA, Mahowald NM (2007) Influence of carbon–nitrogen cycle coupling on land model response to CO2 fertilization and climate variability. Glob Biogeochem Cycles.  https://doi.org/10.1029/2006gb002868 Google Scholar
  118. Tisdall J, Oades J (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163CrossRefGoogle Scholar
  119. Todd-Brown KEO, Hopkins FM, Kivlin SN et al (2011) A framework for representing microbial decomposition in coupled climate models. Biogeochemistry 109:19–33CrossRefGoogle Scholar
  120. Todd-Brown KEO, Randerson JT, Post WM, et al (2013) Causes of variation in soil carbon simulations from CMIP5 Earth system models and comparison with observationsGoogle Scholar
  121. Todd-Brown KEO, Randerson JT, Hopkins F et al (2014) Changes in soil organic carbon storage predicted by Earth system models during the 21st century. Biogeosciences 11:2341–2356CrossRefGoogle Scholar
  122. Torn MS, Trumbore SE, Chadwick OA, Vitousek PM, Hendricks DM (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173CrossRefGoogle Scholar
  123. Torn MS, Swanston CW, Castanha C, Trumbore SE (2009) Storage and turnover of organic matter in soil. In: Biophysico-chemical processes involving natural nonliving organic matter in environmental systems. Wiley, Hoboken, p 219–272Google Scholar
  124. van Ginkel JH, Gorissen A, Polci D (2000) Elevated atmospheric carbon dioxide concentration: effects of increased carbon input in a Lolium perenne soil on microorganisms and decomposition. Soil Biol Biochem 32:449–456CrossRefGoogle Scholar
  125. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  126. Virto I, Barré P, Chenu C (2008) Microaggregation and organic matter storage at the silt-size scale. Geoderma 146:326–335CrossRefGoogle Scholar
  127. von Lützow M, Kögel-Knabner I, Ekschmitt K et al (2007) SOM fractionation methods: relevance to functional pools and to stabilization mechanisms. Soil Biol Biochem 39:2183–2207CrossRefGoogle Scholar
  128. Wang G, Post WM, Mayes MA (2013) Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses. Ecol Appl 23:255–272CrossRefGoogle Scholar
  129. Wang YP, Jiang J, Chen-Charpentier B et al (2016) Responses of two nonlinear microbial models to warming and increased carbon input. Biogeosciences 13:887–902CrossRefGoogle Scholar
  130. Wershaw RL (1986) A new model for humic materials and their interactions with hydrophobic organic chemicals in soil–water or sediment–water systems. J Contam Hydrol 1:29–45CrossRefGoogle Scholar
  131. Wieder WR, Bonan GB, Allison SD (2013) Global soil carbon projections are improved by modelling microbial processes. Nat Clim Change 3:1–7CrossRefGoogle Scholar
  132. Wieder WR, Grandy AS, Kallenbach CM, Bonan GB (2014) Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model. Biogeosciences 11:3899–3917CrossRefGoogle Scholar
  133. Wieder WR, Allison SD, Davidson EA et al (2015a) Explicitly representing soil microbial processes in Earth system models. Glob Biogeochem Cycles 29:1782–1800CrossRefGoogle Scholar
  134. Wieder WR, Grandy AS, Kallenbach CM et al (2015b) Representing life in the Earth system with soil microbial functional traits in the MIMICS model. Geosci Model Dev Discuss 8:2011–2052CrossRefGoogle Scholar
  135. Xu X, Schimel JP, Thornton PE et al (2014) Substrate and environmental controls on microbial assimilation of soil organic carbon: a framework for Earth system models. Ecol Lett 17:547–555CrossRefGoogle Scholar
  136. Young IM, Crawford JW (2004) Interactions and self-organization in the soil–microbe complex. Science 304:1634–1637CrossRefGoogle Scholar
  137. Young IM, Crawford JW, Nunan N, et al (2008) Chapter 4 Microbial Distribution in Soils: Physics and Scaling. In: Advances in Agronomy. Academic Press, pp 81–121Google Scholar
  138. Zaehle S, Medlyn BE, De Kauwe MG et al (2014) Evaluation of 11 terrestrial carbon–nitrogen cycle models against observations from two temperate Free-Air CO2 Enrichment studies. N Phytol 202:803–822CrossRefGoogle Scholar
  139. Zhuang J, McCarthy JF, Perfect E et al (2008) Soil water hysteresis in water-stable microaggregates as affected by organic matter. Soil Sci Soc Am J 72:212–220CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Rose Abramoff
    • 1
    Email author
  • Xiaofeng Xu
    • 2
  • Melannie Hartman
    • 3
  • Sarah O’Brien
    • 4
    • 5
  • Wenting Feng
    • 6
  • Eric Davidson
    • 7
  • Adrien Finzi
    • 8
  • Daryl Moorhead
    • 9
  • Josh Schimel
    • 10
  • Margaret Torn
    • 1
  • Melanie A. Mayes
    • 11
  1. 1.Climate and Ecosystem Sciences DivisionLawrence Berkeley National LaboratoryBerkeleyUSA
  2. 2.Biology DepartmentSan Diego State UniversitySan DiegoUSA
  3. 3.Natural Resource Ecology LaboratoryColorado State UniversityFort CollinsUSA
  4. 4.Biosciences DivisionArgonne National LaboratoryArgonneUSA
  5. 5.Department of Biological SciencesUniversity of Illinois at ChicagoChicagoUSA
  6. 6.Department of Microbiology and Plant BiologyUniversity of OklahomaNormanUSA
  7. 7.Appalachian LaboratoryUniversity of Maryland Center for Environmental ScienceFrostburgUSA
  8. 8.Department of Biology and PhD Program in BiogeoscienceBoston UniversityBostonUSA
  9. 9.Department of Environmental SciencesUniversity of ToledoSt. ToledoUSA
  10. 10.Department of Ecology, Evolution and Marine BiologyUniversity of California Santa BarbaraSanta BarbaraUSA
  11. 11.Environmental Science Division & Climate Change Science InstituteOak Ridge National LaboratoryOak RidgeUSA

Personalised recommendations