Integrating Soil Microbiology into Ecosystem Science

  • David A. LipsonEmail author
  • Xiaofeng Xu
Part of the Advances in Environmental Microbiology book series (AEM, volume 6)


There has been an increasing effort to incorporate the inner workings of soil microbial communities into conceptual and quantitative models of processes at the ecosystem or global scale. Many studies show that the characteristics of microbial species and their interactions with each other and with plants strongly influence larger-scale processes and that explicitly including microbes can improve the performance of ecosystem models. We review the current understanding of how the physiology and community structure of soil microbial communities can impact cycling of carbon (C), nutrients, and greenhouse gases and recent progress in integrating this knowledge into quantitative models of ecosystems and climate change. Microbes can be characterized by ecological strategies that influence carbon use efficiency, stress physiology, elemental ratios (stoichiometry), production of extracellular enzymes, and responses to temperature. Competitive, synergistic, and trophic interactions within soil microbial communities influence process rates and responses to climate change. Plant-microbe interactions are central in climate change responses of ecosystems and can operate by changes in nutrient cycling or through alterations in the balance of mutualists and parasites. There are trends that connect broad-scale community structure with functioning and evidence that ecological roles of microbes can be mapped to phylogeny at the genus or species level. Models that explicitly simulate microbes have included their physiological limits, growth kinetics, interactions with plants, stoichiometry, dormancy, community structure, and community interactions. Given recent advances in conceptual frameworks for microbial ecology and in techniques for describing microbial communities and computing power, further progress will depend on increased interactions between microbiologists and modelers.


Compliance with Ethical Standards

Conflict of Interest

David A. Lipson declares that he has no conflict of interest. Xiaofeng Xu declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. A’Bear AD, Jones TH, Boddy L (2014a) Potential impacts of climate change on interactions among saprotrophic cord-forming fungal mycelia and grazing soil invertebrates. Fungal Ecol 10:34–43CrossRefGoogle Scholar
  2. A’Bear AD, Jones TH, Kandeler E, Boddy L (2014b) Interactive effects of temperature and soil moisture on fungal-mediated wood decomposition and extracellular enzyme activity. Soil Biol Biochem 70:151–158CrossRefGoogle Scholar
  3. Abbott KC, Karst J, Biederman LA, Borrett SR, Hastings A, Walsh V, Bever JD (2015) Spatial heterogeneity in soil microbes alters outcomes of plant competition. PLoS One 10:e0125788PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alexander M (1964) Biochemical ecology of soil microorganisms. Annu Rev Microbiol 18:217–250PubMedCrossRefPubMedCentralGoogle Scholar
  5. Allen A, Schlesinger W (2004) Nutrient limitations to soil microbial biomass and activity in loblolly pine forests. Soil Biol Biochem 36:581–589CrossRefGoogle Scholar
  6. Allen MF, Zink TA (1998) The effects of organic amendments on the restoration of a disturbed coastal sage scrub habitat. Restor Ecol 6:52–58CrossRefGoogle Scholar
  7. Allen B, Willner D, Oechel WC, Lipson DA (2009) Topdown control of microbial activity and biomass in an Arctic soil ecosystem. Environ Microbiol 12:642–648PubMedCrossRefPubMedCentralGoogle Scholar
  8. Allison SD (2012) A trait-based approach for modeling microbial litter decomposition. Ecol Lett 15:1058–1070PubMedCrossRefPubMedCentralGoogle Scholar
  9. Allison SD (2014) Modeling adaptation of carbon use efficiency in microbial communities. Front Microbiol 5:571PubMedPubMedCentralGoogle Scholar
  10. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340CrossRefGoogle Scholar
  11. Anderson T-H, Heinemeyer O, Weigel H-J (2011) Changes in the fungal-to-bacterial respiratory ratio and microbial biomass in agriculturally managed soils under free-air CO2 enrichment (FACE)—a six-year survey of a field study. Soil Biol Biochem 43:895–904CrossRefGoogle Scholar
  12. Austin AT (2011) Has water limited our imagination for aridland biogeochemistry? Trends Ecol Evol 26:229–235PubMedCrossRefGoogle Scholar
  13. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235PubMedCrossRefGoogle Scholar
  14. Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545PubMedCrossRefGoogle Scholar
  15. Ayala-del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N, Bergholz PW, Di Bartolo G, Hauser L, Land M, Bakermans C (2010) The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl Environ Microbiol 76:2304–2312PubMedPubMedCentralCrossRefGoogle Scholar
  16. Baes C, Goeller H, Olson J, Rotty R (1977) Carbon dioxide and climate: the uncontrolled experiment: possibly severe consequences of growing CO 2 release from fossil fuels require a much better understanding of the carbon cycle, climate change, and the resulting impacts on the atmosphere. Am Sci 65:310–320Google Scholar
  17. Bakermans C, Tsapin AI, Souza-Egipsy V, Gilichinsky DA, Nealson KH (2003) Reproduction and metabolism at −10 degrees C of bacteria isolated from Siberian permafrost. Environ Microbiol 5:321–326PubMedCrossRefGoogle Scholar
  18. Bakermans C, Bergholz PW, Rodrigues DF, Vishnivetskaya TA, Ayala-del-Río HL, Tiedje JM (2012) Genomic and expression analyses of cold-adapted microorganisms. In: Miller RV, Whyte LG (eds) Polar microbiology: life in a deep freeze. American Society of Microbiology, Washington, DC, pp 126–155CrossRefGoogle Scholar
  19. Bárcenas-Moreno G, Gómez-Brandón M, Rousk J, Bääth E (2009) Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob Chang Biol 15:2950–2957CrossRefGoogle Scholar
  20. Bellenger J, Xu Y, Zhang X, Morel F, Kraepiel A (2014) Possible contribution of alternative nitrogenases to nitrogen fixation by asymbiotic N 2-fixing bacteria in soils. Soil Biol Biochem 69:413–420CrossRefGoogle Scholar
  21. Bennett AF, Lenski RE (1993) Evolutionary adaptation to temperature II. Thermal niches of experimental lines of Escherichia coli. Evolution 47(1):12CrossRefGoogle Scholar
  22. Bier RL, Bernhardt ES, Boot CM, Graham EB, Hall EK, Lennon JT, Nemergut DR, Osborne BB, Ruiz-González C, Schimel JP, Waldrop MP, Wallenstein MD, Muyzer G (2015) Linking microbial community structure and microbial processes: an empirical and conceptual overview. FEMS Microbiol Ecol 91:fiv113PubMedCrossRefPubMedCentralGoogle Scholar
  23. Bloom AA, Palmer PI, Fraser A, Reay DS, Frankenberg C (2010) Large-scale controls of methanogenesis inferred from methane and gravity spaceborne data. Science 327:322–325PubMedCrossRefPubMedCentralGoogle Scholar
  24. Bowker MA, Maestre FT, Eldridge D, Belnap J, Castillo-Monroy A, Escolar C, Soliveres S (2014) Biological soil crusts (biocrusts) as a model system in community, landscape and ecosystem ecology. Biodivers Conserv 23:1619–1637CrossRefGoogle Scholar
  25. Bozzolo FH, Lipson DA (2013) Differential responses of native and exotic coastal sage scrub plant species to N additions and the soil microbial community. Plant Soil 371:37–51CrossRefGoogle Scholar
  26. Bradford MA (2013) Thermal adaptation of decomposer communities in warming soils. Front Microbiol 4:333PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327PubMedCrossRefPubMedCentralGoogle Scholar
  28. Brooks P, Williams MW, Schmidt SK (1996) Microbial activity under alpine snowpacks, Niwot Ridge, Colorado. Biogeochemistry 32:93–113CrossRefGoogle Scholar
  29. Brooks PD, Schmidt SK, Williams MW (1997) Winter production of CO2 and N2O from alpine tundra: environmental controls and relationship to inter-system C and N fluxes. Oecologia 110:403–413PubMedPubMedCentralGoogle Scholar
  30. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  31. Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055PubMedCrossRefPubMedCentralGoogle Scholar
  32. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522PubMedCrossRefPubMedCentralGoogle Scholar
  33. Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007PubMedCrossRefGoogle Scholar
  34. Castro-Díez P, Godoy O, Alonso A, Gallardo A, Saldaña A (2014) What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol Lett 17:1–12PubMedCrossRefPubMedCentralGoogle Scholar
  35. Chapin FS, McFarland J, McGuire AD, Euskirchen ES, Ruess RW, Kielland K (2009) The changing global carbon cycle: linking plant–soil carbon dynamics to global consequences. J Ecol 97:840–850CrossRefGoogle Scholar
  36. Chau JF, Bagtzoglou AC, Willig MR (2011) The effect of soil texture on richness and diversity of bacterial communities. Environ Forensic 12:333–341CrossRefGoogle Scholar
  37. Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quéré C, Myneni RB, Piao S, Thornton P (2013) Carbon and other biogeochemical cycles. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  38. Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere 6:art130CrossRefGoogle Scholar
  39. Clein JS, Schimel JP (1995) Microbial activity of tundra and taiga soils at sub-zero temperatures. Soil Biol Biochem 27:1231–1234CrossRefGoogle Scholar
  40. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  41. Cleveland CC, Townsend AR, Schmidt SK (2002) Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems 5:0680–0691CrossRefGoogle Scholar
  42. Coleman K, Jenkinson D (1996) RothC-26.3-A model for the turnover of carbon in soil. In: Evaluation of soil organic matter models. Springer, Heidelberg, pp 237–246CrossRefGoogle Scholar
  43. Collier FA, Bidartondo MI (2009) Waiting for fungi: the ectomycorrhizal invasion of lowland heathlands. J Ecol 97:950–963CrossRefGoogle Scholar
  44. Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH (2008) Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–420CrossRefGoogle Scholar
  45. 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 19:988–995PubMedCrossRefPubMedCentralGoogle Scholar
  46. Cowan DA (2004) The upper temperature for life–where do we draw the line? Trends Microbiol 12:58–60CrossRefGoogle Scholar
  47. Crowther TW, Thomas SM, Maynard DS, Baldrian P, Covey K, Frey SD, van Diepen LTA, Bradford MA (2015) Biotic interactions mediate soil microbial feedbacks to climate change. Proc Natl Acad Sci USA 112:7033–7038PubMedCrossRefPubMedCentralGoogle Scholar
  48. da Rocha UN, Plugge CM, George I, van Elsas JD, van Overbeek LS (2013) The rhizosphere selects for particular groups of acidobacteria and verrucomicrobia. PLoS One 8:e82443CrossRefGoogle Scholar
  49. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Ba A, Burla S, Diedhiou A, Hiiesalu I, Jairus T (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973PubMedCrossRefPubMedCentralGoogle Scholar
  50. de Vries FT, Bardgett RD (2012) Plant–microbial linkages and ecosystem nitrogen retention: lessons for sustainable agriculture. Front Ecol Environ 10:425–432CrossRefGoogle Scholar
  51. de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265PubMedPubMedCentralCrossRefGoogle Scholar
  52. DeAngelis KM, Pold G, Topçuoğlu BD, van Diepen LT, Varney RM, Blanchard JL, Melillo J, Frey SD (2015) Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6:104PubMedPubMedCentralCrossRefGoogle Scholar
  53. Del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541CrossRefGoogle Scholar
  54. Delgado-Baquerizo M, Maestre FT, Rodríguez JG, Gallardo A (2013) Biological soil crusts promote N accumulation in response to dew events in dryland soils. Soil Biol Biochem 62:22–27CrossRefGoogle Scholar
  55. DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50:470–478PubMedCrossRefPubMedCentralGoogle Scholar
  56. DeLong EF, Harwood CS, Chisholm PW, Karl DM, Moran MA, Schmidt TM, Tiedje JM, Treseder KK, Worden AZ (2011) Incorporating microbial processes into climate models. The American Academy of Microbiology, Washington, DCGoogle Scholar
  57. Dieleman WIJ, Vicca S, Dijkstra FA, Hagedorn F, Hovenden MJ, Larsen KS, Morgan JA, Volder A, Beierk C, Dukes JS, King J, Leuzinger S, Linder S, Luo YQ, Oren R, Angelis PD, Tingey D, Hoosbeek MR, Janssens IA (2012) Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob Chang Biol 18:2681–2693PubMedCrossRefPubMedCentralGoogle Scholar
  58. Diez JM, James TY, McMunn M, Ibáñez I (2013) Predicting species-specific responses of fungi to climatic variation using historical records. Glob Chang Biol 19:3145–3154PubMedCrossRefPubMedCentralGoogle Scholar
  59. Dijkstra P, Thomas SC, Heinrich PL, Koch GW, Schwartz E, Hungate BA (2011) Effect of temperature on metabolic activity of intact microbial communities: evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency. Soil Biol Biochem 43:2023–2031CrossRefGoogle Scholar
  60. Dijkstra FA, Augustine DJ, Brewer P, von Fischer JC (2012) Nitrogen cycling and water pulses in semiarid grasslands: are microbial and plant processes temporally asynchronous? Oecologia 170:799–808PubMedCrossRefPubMedCentralGoogle Scholar
  61. Docherty KM, Borton HM, Espinosa N, Gebhardt M, Gil-Loaiza J, Gutknecht JLM, Maes PW, Mott BM, Parnell JJ, Purdy G, Rodrigues PAP, Stanish LF, Walser ON, Gallery RE (2015) Key edaphic properties largely explain temporal and geographic variation in soil microbial communities across four biomes. PLoS One 10:e0135352PubMedPubMedCentralCrossRefGoogle Scholar
  62. Dziewit L, Bartosik D (2014) Plasmids of psychrophilic and psychrotolerant bacteria and their role in adaptation to cold environments. Front Microbiol 5:596PubMedPubMedCentralCrossRefGoogle Scholar
  63. Evans SE, Wallenstein MD (2014) Climate change alters ecological strategies of soil bacteria. Ecol Lett 17:155–164PubMedCrossRefPubMedCentralGoogle Scholar
  64. Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039PubMedCrossRefPubMedCentralGoogle Scholar
  65. Fanin N, Fromin N, Buatois B, Hättenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter–microbe system. Ecol Lett 16:764–772PubMedCrossRefPubMedCentralGoogle Scholar
  66. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550PubMedCrossRefPubMedCentralGoogle Scholar
  67. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208PubMedCrossRefPubMedCentralGoogle Scholar
  68. Ferris H, Tuomisto H (2015) Unearthing the role of biological diversity in soil health. Soil Biol Biochem 85:101–109CrossRefGoogle Scholar
  69. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631PubMedCrossRefPubMedCentralGoogle Scholar
  70. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedCrossRefPubMedCentralGoogle Scholar
  71. Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249PubMedCrossRefPubMedCentralGoogle Scholar
  72. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci 109:21390–21395PubMedCrossRefPubMedCentralGoogle Scholar
  73. Finzi AC, Norby RJ, Calfapietra C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Iversen CM, Jackson RB, Kubiske ME (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci USA 104:14014–14019PubMedCrossRefPubMedCentralGoogle Scholar
  74. Folse HJ, Allison SD (2012) Cooperation, competition, and coalitions in enzyme-producing microbes: social evolution and nutrient depolymerization rates. Front Microbiol 3:338PubMedPubMedCentralCrossRefGoogle Scholar
  75. Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96CrossRefGoogle Scholar
  76. Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store. Nature 409:149–149PubMedCrossRefPubMedCentralGoogle Scholar
  77. Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3:395–398CrossRefGoogle Scholar
  78. García-Palacios P, Vandegehuchte ML, Shaw EA, Dam M, Post KH, Ramirez KS, Sylvain ZA, de Tomasel CM, Wall DH (2015) Are there links between responses of soil microbes and ecosystem functioning to elevated CO2, N deposition and warming? A global perspective. Glob Chang Biol 21:1590–1600PubMedCrossRefPubMedCentralGoogle Scholar
  79. Gehring CA, Mueller RC, Haskins KE, Rubow TK, Whitham TG (2014) Convergence in mycorrhizal fungal communities due to drought, plant competition, parasitism, and susceptibility to herbivory: consequences for fungi and host plants. Front Microbiol 5:306PubMedPubMedCentralCrossRefGoogle Scholar
  80. George IF, Hartmann M, Liles MR, Agathos SN (2011) Recovery of as-yet-uncultured soil Acidobacteria on dilute solid media. Appl Environ Microbiol 77:8184–8188PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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 Chang Biol 18:1468–1479CrossRefGoogle Scholar
  82. Giardina CP, Ryan MG (2000) Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404:858–861PubMedCrossRefPubMedCentralGoogle Scholar
  83. Giles M, Morley N, Baggs EM, Daniell TJ (2012) Soil nitrate reducing processes—drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front Microbiol 3:407PubMedPubMedCentralCrossRefGoogle Scholar
  84. Gillooly JF, Allen AP, Brown JH, Elser JJ, del Rio CM, Savage VM, West GB, Woodruff WH, Woods HA (2005) The metabolic basis of whole-organism RNA and phosphorus content. Proc Natl Acad Sci USA 102:11923–11927PubMedCrossRefPubMedCentralGoogle Scholar
  85. Glass JB, Orphan VJ (2012) Trace metal requirements for microbial enzymes involved in the production and consumption of methane and nitrous oxide. Front Microbiol 3:61PubMedPubMedCentralGoogle Scholar
  86. Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:94PubMedPubMedCentralCrossRefGoogle Scholar
  87. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129PubMedCrossRefPubMedCentralGoogle Scholar
  88. Grzymski JJ, Carter BJ, DeLong EF, Feldman RA, Ghadiri A, Murray AE (2006) Comparative genomics of DNA fragments from six Antarctic marine planktonic bacteria. Appl Environ Microbiol 72:1532–1541PubMedPubMedCentralCrossRefGoogle Scholar
  89. Hagerty SB, van Groenigen KJ, Allison SD, Hungate BA, Schwartz E, Koch GW, Kolka RK, Dijkstra P (2014) Accelerated microbial turnover but constant growth efficiency with warming in soil. Nat Clim Chang 4:903–906CrossRefGoogle Scholar
  90. Hahn MW, Pöckl M (2005) Ecotypes of planktonic Actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats. Appl Environ Microbiol 71:766–773PubMedPubMedCentralCrossRefGoogle Scholar
  91. Hanus F, Morita RY (1968) Significance of the temperature characteristic of growth. J Bacteriol 95:736PubMedPubMedCentralGoogle Scholar
  92. Hararuk O, Smith MJ, Luo Y (2015) Microbial models with data-driven parameters predict stronger soil carbon responses to climate change. Glob Chang Biol 21:2439–2453PubMedCrossRefPubMedCentralGoogle Scholar
  93. Hartman WH, Richardson CJ (2013) Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO2): is there a biological stoichiometry of soil microbes? PLoS One 8:e57127PubMedPubMedCentralCrossRefGoogle Scholar
  94. He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, Van Nostrand JD, Hobbie SE, Reich PB, Zhou J (2010) Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett 13:564–575PubMedCrossRefPubMedCentralGoogle Scholar
  95. Henry HAL (2013) Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem 56:53–59CrossRefGoogle Scholar
  96. Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129CrossRefGoogle Scholar
  97. Hines ME, Duddleston KN, Rooney-Varga JN, Fields D, Chanton JP (2008) Uncoupling of acetate degradation from methane formation in Alaskan wetlands: connections to vegetation distribution. Glob Biogeochem Cycles 22:GB2017. CrossRefGoogle Scholar
  98. Högberg M, Högberg P, Myrold D (2007a) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three. Oecologia 150:590–601PubMedCrossRefPubMedCentralGoogle Scholar
  99. Högberg MN, Chen Y, Högberg P (2007b) Gross nitrogen mineralisation and fungi-to-bacteria ratios are negatively correlated in boreal forests. Biol Fertil Soils 44:363–366CrossRefGoogle Scholar
  100. Huston AL, Krieger-Brockett BB, Deming JW (2000) Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria and sea ice. Environ Microbiol 2:383–388PubMedCrossRefPubMedCentralGoogle Scholar
  101. Inglima I, Alberti G, Bertolini T, Vaccari F, Gioli B, Miglietta F, Cotrufo M, Peressotti A (2009) Precipitation pulses enhance respiration of Mediterranean ecosystems: the balance between organic and inorganic components of increased soil CO2 efflux. Glob Chang Biol 15:1289–1301CrossRefGoogle Scholar
  102. Jaspers E, Overmann J (2004) Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70:4831–4839PubMedPubMedCentralCrossRefGoogle Scholar
  103. Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry. Academic Press, Dekker, New York, pp 415–472Google Scholar
  104. Jenkinson DS, Hart PBS, Rayner JH, Parry LC (1987) Modelling the turnover of organic matter in long-term experiments at Rothamstedt. INTECOL Bulletin 15:1–8Google Scholar
  105. Jiang X, Hou X, Zhou X, Xin X, Wright A, Jia Z (2015) pH regulates key players of nitrification in paddy soils. Soil Biol Biochem 81:9–16CrossRefGoogle Scholar
  106. Johnson SL, Kuske CR, Carney TD, Housman DC, Gallegos-Graves LV, Belnap J (2012) Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Glob Chang Biol 18:2583–2593CrossRefGoogle Scholar
  107. Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV (1996) Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake. Oecologia 106:507–515PubMedCrossRefPubMedCentralGoogle Scholar
  108. Jones CM, Graf DRH, Bru D, Philippot L, Hallin S (2012) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426PubMedPubMedCentralCrossRefGoogle Scholar
  109. Kaiser C, Franklin O, Dieckmann U, Richter A (2014) Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett 17:680–690PubMedPubMedCentralCrossRefGoogle Scholar
  110. Kaiser C, Franklin O, Richter A, Dieckmann U (2015) Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils. Nat Commun 6:8960PubMedPubMedCentralCrossRefGoogle Scholar
  111. Keiblinger KM, Hall EK, Wanek W, Szukics U, Hämmerle I, Ellersdorfer G, Böck S, Strauss J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440PubMedGoogle Scholar
  112. Keller JK, Weisenhorn PB, Megonigal JP (2009) Humic acids as electron acceptors in wetland decomposition. Soil Biol Biochem 41:1518–1522CrossRefGoogle Scholar
  113. Kreft JU, Bonhoeffer S (2005) The evolution of groups of cooperating bacteria and the growth rate versus yield trade-off. Microbiology 151:637–641PubMedCrossRefGoogle Scholar
  114. Kuhn E (2012) Toward understanding life under subzero conditions: the significance of exploring psychrophilic “cold-shock” proteins. Astrobiology 12:1078–1086PubMedCrossRefGoogle Scholar
  115. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199CrossRefGoogle Scholar
  116. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669PubMedCrossRefGoogle Scholar
  117. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821PubMedPubMedCentralCrossRefGoogle Scholar
  118. Lankau RA, Zhu K, Ordonez A (2015) Mycorrhizal strategies of tree species correlate with trailing range edge responses to current and past climate change. Ecology 96:1451–1458CrossRefGoogle Scholar
  119. Lawrence CR, Neff JC, Schimel JP (2009) 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 41:1923–1934CrossRefGoogle Scholar
  120. Le Mer J, Roger P (2001) Production, oxidation, emission and consumption of methane by soils: a review. Eur J Soil Biol 37:25–50CrossRefGoogle Scholar
  121. Legay N, Baxendale C, Grigulis K, Krainer U, Kastl E, Schloter M, Bardgett RD, Arnoldi C, Bahn M, Dumont M, Poly F, Pommier T, Clément JC, Lavorel S (2014) Contribution of above- and below-ground plant traits to the structure and function of grassland soil microbial communities. Ann Bot 114:1011–1021PubMedPubMedCentralCrossRefGoogle Scholar
  122. Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714PubMedCrossRefGoogle Scholar
  123. Lipson DA (2007) Relationships between temperature responses and bacterial community structure along seasonal and altitudinal gradients. FEMS Microbiol Ecol 59:418–427PubMedCrossRefGoogle Scholar
  124. Lipson DA (2015) The complex relationship between microbial growth rate and yield and its implications for ecosystem processes. Front Microbiol 6:615PubMedPubMedCentralGoogle Scholar
  125. Lipson DA, Kelley ST (2014) Plant-microbe interactions. In: Monson RK (ed) Ecology and the environment. Springer, New York, pp 177–204Google Scholar
  126. Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and N availability in an alpine ecosystem. Ecology 80:1623–1631CrossRefGoogle Scholar
  127. Lipson DA, Wilson RF, Oechel WC (2005) Effects of elevated atmospheric CO2 on soil microbial biomass, activity and diversity in a chaparral ecosystem. Appl Environ Microbiol 71:8573–8580PubMedPubMedCentralCrossRefGoogle Scholar
  128. Lipson DA, Monson RK, Schmidt SK, Weintraub MN (2009) The trade-off between growth rate and yield in microbial communities and the consequences for under-snow soil respiration in a high elevation coniferous forest. Biogeochemistry 95:23–35CrossRefGoogle Scholar
  129. Lipson DA, Kuske CR, Gallegos-Graves LV, Oechel WC (2014) Elevated atmospheric CO2 stimulates soil fungal diversity through increased fine root production in a semiarid shrubland ecosystem. Glob Chang Biol 20:2555–2565PubMedCrossRefGoogle Scholar
  130. Long A, Heitman J, Tobias C, Philips R, Song B (2012) Co-occurring anammox, denitrification, and codenitrification in agricultural soils. Appl Environ Microbiol 79:168–176PubMedCrossRefGoogle Scholar
  131. Lovley DR, Phillips EJP (1987) Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Appl Environ Microbiol 53:2636–2641PubMedPubMedCentralGoogle Scholar
  132. Luo YQ, Wan SQ, Hui DF, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625PubMedCrossRefGoogle Scholar
  133. Luo Y, Ahlström A, Allison SD, Batjes NH, Brovkin V, Carvalhais N, Chappell A, Ciais P, Davidson EA, Finzi A, Georgiou K, Guenet B, Hararuk O, Harden JW, He Y, Hopkins FM, Jiang L, Koven CD, Jackson RB, Jones CD, Lara MJ, Liang J, McGuire AD, Parton W, Peng C, Randerson JT, Salazar A, sierra CA, Smith M, Tian H, Todd-Brown KE, Torn M, van Groenendael J, Wang Y-P, West TO, Wei Y, Wieder WR, Xia J, Xu X, Xu X, Zhou T (2016) Towards more realistic projections of soil carbon dynamics by earth system models. Glob Biogeochem Cycles 30:40–56. CrossRefGoogle Scholar
  134. Lynch MD, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229PubMedCrossRefGoogle Scholar
  135. Maida I, Bosi E, Perrin E, Papaleo MC, Orlandini V, Fondi M, Fani R, Wiegel J, Bianconi G, Canganella F (2013) Draft genome sequence of the fast-growing bacterium Vibrio natriegens strain DSMZ 759. Genome Announc 1:e00648–e00613PubMedPubMedCentralCrossRefGoogle Scholar
  136. Manzoni S, Porporato A (2009) Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biol Biochem 41(7):1355–1379CrossRefGoogle Scholar
  137. Manzoni S, Taylor P, Richter A, Porporato A, Ågren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91PubMedCrossRefGoogle Scholar
  138. Manzoni S, Schaeffe SM, Katul G, Porporato A, Schimel J (2014) A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biol Biochem 73:69–83CrossRefGoogle Scholar
  139. Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361PubMedCrossRefGoogle Scholar
  140. McCalley CK, Woodcroft BJ, Hodgkins SB, Wehr RA, Kim E-H, Mondav R, Crill PM, Chanton JP, Rich VI, Tyson GW (2014) Methane dynamics regulated by microbial community response to permafrost thaw. Nature 514:478–481PubMedCrossRefGoogle Scholar
  141. McCann KS (2000) The diversity–stability debate. Nature 405:228–233PubMedCrossRefGoogle Scholar
  142. Melton J, Wania R, Hodson E, Poulter B, Ringeval B, Spahni R, Bohn T, Avis C, Beerling D, Chen G (2013) Present state of global wetland extent and wetland methane modelling: conclusions from a model intercomparison project (WETCHIMP). Biogeosciences 10:753–788CrossRefGoogle Scholar
  143. Mikan CJ, Schimel JP, Doyle AP (2002) Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biol Biochem 34:1785–1795CrossRefGoogle Scholar
  144. Miller KE, Lai C-T, Friedman ES, Angenent LT, Lipson DA (2015) Methane suppression by iron and humic acids in soils of the arctic coastal plain. Soil Biol Biochem 83:176–183CrossRefGoogle Scholar
  145. Monson RK, Lipson DA, Burns SP, Turnipseed AA, Delany AC, Williams MW, Schmidt SK (2006) Forest soil respiration controlled by winter climate variation and microbial community composition. Nature 439:711–714PubMedCrossRefGoogle Scholar
  146. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174CrossRefGoogle Scholar
  147. 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
  148. Moorhead D, Lashermes G, Recous S, Bertrand I (2014) Interacting microbe and litter quality controls on litter decomposition: a modeling analysis. PloS One 9:e108769PubMedPubMedCentralCrossRefGoogle Scholar
  149. Morel F, Price N (2003) The biogeochemical cycles of trace metals in the oceans. Science 300:944–947PubMedCrossRefGoogle Scholar
  150. Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144PubMedPubMedCentralGoogle Scholar
  151. Mothapo N, Chen H, Cubeta MA, Grossman JM, Fuller F, Shi W (2015) Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy. Soil Biol Biochem 83:160–175CrossRefGoogle Scholar
  152. Myhre G, Shindell D, Bréon F, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J, Lee D, Mendoza B (2013) Anthropogenic and natural radiative forcing. In: Climate change 2013: the physical science basis. Contribution of Working Group 1 to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Table 8, p 714Google Scholar
  153. Nam H, Lewis NE, Lerman JA, Lee D-H, Chang RL, Kim D, Palsson BO (2012) Network context and selection in the evolution to enzyme specificity. Science 337:1101–1104PubMedPubMedCentralCrossRefGoogle Scholar
  154. Nazaries L, Murrell JC, Millard P, Baggs L, Singh BK (2013) Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions. Environ Microbiol 15:2395–2417PubMedCrossRefGoogle Scholar
  155. Nemergut DR, Shade A, Violle C (2014) When, where and how does microbial community composition matter? Front Microbiol 5:424PubMedPubMedCentralCrossRefGoogle Scholar
  156. Neuenschwander SM, Pernthaler J, Posch T, Salcher MM (2015) Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. Environ Microbiol 17:781–795PubMedCrossRefGoogle Scholar
  157. Nielsen U, Ayres E, Wall D, Bardgett R (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62:105–116CrossRefGoogle Scholar
  158. Nielsen UN, Wall DH, Six J (2015) Soil biodiversity and the environment. Annu Rev Environ Resour 40:63–90CrossRefGoogle Scholar
  159. Osanai Y, Janes JK, Newton PCD, Hovenden MJ (2015) Warming and elevated CO2 combine to increase microbial mineralisation of soil organic matter. Soil Biol Biochem 85:110–118CrossRefGoogle Scholar
  160. Pan Y, Ni B-J, Bond PL, Ye L, Yuan Z (2013) Electron competition among nitrogen oxides reduction during methanol-utilizing denitrification in wastewater treatment. Water Res 47:3273–3281PubMedCrossRefGoogle Scholar
  161. Panikov N (2009) Microbial activity in frozen soils. In: Margesin R (ed) Permafrost soils. Springer, Berlin, pp 119–147CrossRefGoogle Scholar
  162. Panikov NS, Flanagan PW, Oechel WC, Mastepanov MA, Christensen TR (2006) Microbial activity in soils frozen to below −39°C. Soil Biol Biochem 38:785–794CrossRefGoogle Scholar
  163. Parton WJ, Schimel DS, Cole CV, Ojima DS (1987) Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci Soc Am J 51:1173–1179CrossRefGoogle Scholar
  164. Peay KG, Garbelotto M, Bruns TD (2010) Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. Ecology 91:3631–3640PubMedCrossRefGoogle Scholar
  165. Pelini SL, Maran AM, Chen AR, Kaseman J, Crowther TW (2015) Higher trophic levels overwhelm climate change impacts on terrestrial ecosystem functioning. PLoS One 10:e0136344PubMedPubMedCentralCrossRefGoogle Scholar
  166. Philippot L, Andersson SGE, Battin TJ, Prosser JI, Schimel JP, Whitman WB, Hallin S (2010) The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8:523–529PubMedCrossRefGoogle Scholar
  167. Pietikäinen J, Pettersson M, Baath E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58PubMedCrossRefGoogle Scholar
  168. Piette F, D’Amico S, Struvay C, Mazzucchelli G, Renaut J, Tutino ML, Danchin A, Leprince P, Feller G (2010) Proteomics of life at low temperatures: trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Mol Microbiol 76:120–132PubMedCrossRefGoogle Scholar
  169. Placella SA, Brodie EL, Firestone MK (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci USA 109:10931–10936PubMedCrossRefGoogle Scholar
  170. Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, Op den Camp HJM (2007) Methanotrophy below pH1 by a new Verrucomicrobia species. Nature 450:874–878PubMedCrossRefGoogle Scholar
  171. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394PubMedCrossRefGoogle Scholar
  172. Ratkowsky D, Olley J, McMeekin T, Ball A (1982) Relationship between temperature and growth rate of bacterial cultures. J Bacteriol 149:1–5PubMedPubMedCentralGoogle Scholar
  173. Ratkowsky D, Lowry R, McMeekin T, Stokes A, Chandler R (1983) Model for bacterial culture growth rate throughout the entire biokinetic temperature range. J Bacteriol 154:1222–1226PubMedPubMedCentralGoogle Scholar
  174. Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221Google Scholar
  175. Robador A, Müller AL, Sawicka JE, Berry D, Hubert CRJ, Loy A, Jørgensen BB, Brüchert V (2015) Activity and community structures of sulfate-reducing microorganisms in polar, temperate and tropical marine sediments. ISME J 10:796–809PubMedPubMedCentralCrossRefGoogle Scholar
  176. Roco CA, Bergaust LL, Bakken LR, Yavitt JB, Shapleigh JP (2016) Modularity of nitrogen-oxide reducing soil bacteria: linking phenotype to genotype. Environ Microbiol 19(6):2507–2519PubMedCrossRefPubMedCentralGoogle Scholar
  177. Rodrigues DF, da C Jesus E, Ayala-del-Río HL, Pellizari VH, Gilichinsky D, Sepulveda-Torres L, Tiedje JM (2009) Biogeography of two cold-adapted genera: psychrobacter and Exiguobacterium. ISME J 3:658–665PubMedCrossRefPubMedCentralGoogle Scholar
  178. Rotaru A-E, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin K, Lovley D (2014) Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol 80(15):4599–4605PubMedPubMedCentralCrossRefGoogle Scholar
  179. Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30PubMedCrossRefPubMedCentralGoogle Scholar
  180. Rousk J, Frey SD, Bååth E (2012) Temperature adaptation of bacterial communities in experimentally warmed forest soils. Glob Chang Biol 18:3252–3258PubMedCrossRefPubMedCentralGoogle Scholar
  181. Sakamoto K, Oba Y (1994) Effect of fungal to bacterial biomass ratio on the relationship between CO2 evolution and total soil microbial biomass. Biol Fertil Soils 17:39–44CrossRefGoogle Scholar
  182. Salvadó Z, Arroyo-López F, Guillamón JM, Salazar G, Querol A, Barrio E (2011) Temperature adaptation markedly determines evolution within the genus Saccharomyces. Appl Environ Microbiol 77:2292–2302PubMedPubMedCentralCrossRefGoogle Scholar
  183. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-Garcia C, Rodriguez G, Massol-Deya A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Loffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci USA 109:19709–19714PubMedCrossRefPubMedCentralGoogle Scholar
  184. Schaefer K, Lantuit H, Romanovsky VE, Schuur EAG, Witt R (2014) The impact of the permafrost carbon feedback on global climate. Environ Res Lett 9:085003CrossRefGoogle Scholar
  185. Schimel J (1995) Ecosystem consequences of microbial diversity and community structure. In: Arctic and alpine biodiversity: patterns, causes and ecosystem consequences. Springer, Berlin, pp 239–254Google Scholar
  186. Schimel JP (2001) Biogeochemical models: implicit vs. explicit microbiology. In: Schulze E-D (ed) Global biogeochemical cycles in the climate systems. Academic Press, New York, pp 177–183CrossRefGoogle Scholar
  187. Schimel JP, Gulledge J (1998) Microbial community structure and global trace gases. Glob Chang Biol 4:745–758CrossRefGoogle Scholar
  188. Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348PubMedPubMedCentralCrossRefGoogle Scholar
  189. 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
  190. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394PubMedCrossRefPubMedCentralGoogle Scholar
  191. Schmidt SK, Wilson KL, Monson RK, Lipson DA (2009) Exponential growth of “snow molds” at sub-zero temperatures: an explanation for high beneath-snow respiration rates and Q 10 values. Biogeochemistry 95:13–21CrossRefGoogle Scholar
  192. Schuur EAG, McGuire AD, Schädel C, Grosse G, Harden JW, Hayes DJ, Hugelius G, Koven CD, Kuhry P, Lawrence DM, Natali SM, Olefeldt D, Romanovsky VE, Schaefer K, Turetsky MR, Treat CC, Vonk JE (2015) Climate change and the permafrost carbon feedback. Nature 520:171–179PubMedCrossRefPubMedCentralGoogle Scholar
  193. Scott-Denton LE, Rosenstiel T, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Chang Biol 12:205–216CrossRefGoogle Scholar
  194. Sigüenza C, Corkidi L, Allen EB (2006) Feedbacks of soil inoculum of mycorrhizal fungi altered by N deposition on the growth of a native shrub and an invasive annual grass. Plant Soil 286:153–165CrossRefGoogle Scholar
  195. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  196. Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939PubMedCrossRefPubMedCentralGoogle Scholar
  197. Sinsabaugh RL, Shah JJF, Findlay SG, Kuehn KA, Moorhead DL (2014) Scaling microbial biomass, metabolism and resource supply. Biogeochemistry 122:175–190CrossRefGoogle Scholar
  198. Sinsabaugh RL, Turner BL, Talbot JM, Waring BG, Powers JS, Kuske CR, Moorhead DL, Follstad Shah JJ (2016) Stoichiometry of microbial carbon use efficiency in soils. Ecol Monogr 86(2):172–189CrossRefGoogle Scholar
  199. Sistla SA, Asao S, Schimel JP (2012) Detecting microbial N-limitation in tussock tundra soil: implications for Arctic soil organic carbon cycling. Soil Biol Biochem 55:78–84CrossRefGoogle Scholar
  200. 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(1):151–170CrossRefGoogle Scholar
  201. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569CrossRefGoogle Scholar
  202. Smemo K, Yavitt J (2011) Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems? Biogeosciences 8:779–793CrossRefGoogle Scholar
  203. Spencer SJ, Tamminen MV, Preheim SP, Guo MT, Briggs AW, Brito IL, Weitz DA, Pitkänen LK, Vigneault F, Virta MP (2015) Massively parallel sequencing of single cells by epicPCR links functional genes with phylogenetic markers. ISME J 0(2):427–436CrossRefGoogle Scholar
  204. Spohn M, Chodak M (2015) Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biol Biochem 81:128–133CrossRefGoogle Scholar
  205. Staley JT, Castenholz RW, Colwell RR, Holt JG, Kane MD, Pace NR, Salyers AA, Tiedje JMT (1997) The microbial world. American Society for Microbiology, Washington, DCGoogle Scholar
  206. Stein LY, Klotz MG (2016) The nitrogen cycle. Curr Biol 26:R94–R98PubMedCrossRefPubMedCentralGoogle Scholar
  207. Steinauer K, Tilman D, Wragg PD, Cesarz S, Cowles JM, Pritsch K, Reich PB, Weisser WW, Eisenhauer N (2015) Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology 96:99–112PubMedCrossRefPubMedCentralGoogle Scholar
  208. Steinweg JM, Plante AF, Conant RT, Paul EA, Tanaka DL (2008) Patterns of substrate utilization during long-term incubations at different temperatures. Soil Biol Biochem 40:2722–2728CrossRefGoogle Scholar
  209. Steven B, Leveille R, Pollard WH, Whyte LG (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267PubMedCrossRefPubMedCentralGoogle Scholar
  210. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160PubMedPubMedCentralCrossRefGoogle Scholar
  211. Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, Schleper C (2014) Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8:1135–1146PubMedPubMedCentralCrossRefGoogle Scholar
  212. Sulman BN, Phillips RP, Oishi AC, Shevliakova E, Pacala SW (2014) Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nat Clim Chang 4:1099–1102CrossRefGoogle Scholar
  213. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963CrossRefGoogle Scholar
  214. Tang J, Riley WJ (2015) Weaker soil carbon-climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Chang 5:56–60CrossRefGoogle Scholar
  215. Thiet RK, Frey SD, Six J (2006) Do growth yield efficiencies differ between soil microbial communities differing in fungal: bacterial ratios? Reality check and methodological issues. Soil Biol Biochem 38:837–844CrossRefGoogle Scholar
  216. Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD (2011) A framework for representing microbial decomposition in coupled climate models. Biogeochemistry 109:19–33CrossRefGoogle Scholar
  217. Travisano M, Velicer GJ (2004) Strategies of microbial cheater control. Trends Microbiol 12:72–78PubMedCrossRefPubMedCentralGoogle Scholar
  218. Treseder KK, Balser TC, Bradford MA, Brodie EL, Dubinsky EA, Eviner VT, Hofmockel KS, Lennon JT, Levine UY, MacGregor BJ (2012) Integrating microbial ecology into ecosystem models: challenges and priorities. Biogeochemistry 109:7–18CrossRefGoogle Scholar
  219. Tucker CL, Bell J, Pendall E, Ogle K (2013) Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob Chang Biol 19:252–263PubMedCrossRefPubMedCentralGoogle Scholar
  220. Tveit AT, Urich T, Frenzel P, Svenning MM (2015) Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming. Proc Natl Acad Sci USA 112:E2507–E2516PubMedCrossRefPubMedCentralGoogle Scholar
  221. Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedCrossRefPubMedCentralGoogle Scholar
  222. van der Putten WH, Bradford MA, Brinkman EP, van de Voorde TF, Veen G (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121CrossRefGoogle Scholar
  223. van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci USA 109:1159–1164PubMedCrossRefPubMedCentralGoogle Scholar
  224. Van Veen J, Ladd J, Frissel M (1984) Modelling C and N turnover through the microbial biomass in soil. Plant Soil 76:257–274CrossRefGoogle Scholar
  225. Veen JV, Paul E (1981) Organic carbon dynamics in grassland soils. 1. Background information and computer simulation. Can J Soil Sci 61:185–201CrossRefGoogle Scholar
  226. von Fischer JC, Rhew RC, Ames GM, Fosdick BK, von Fischer PE (2010) Vegetation height and other controls of spatial variability in methane emissions from the Arctic coastal tundra at Barrow, Alaska. J Geophys Res 115:G00I03. CrossRefGoogle Scholar
  227. Wagai R, Kishimoto-Mo AW, Yonemura S, Shirato Y, Hiradate S, Yagasaki Y (2013) Linking temperature sensitivity of soil organic matter decomposition to its molecular structure, accessibility, and microbial physiology. Glob Chang Biol 19:1114–1125PubMedCrossRefPubMedCentralGoogle Scholar
  228. Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177CrossRefGoogle Scholar
  229. Wallenstein MD, Hall EK (2012) A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109:35–47CrossRefGoogle Scholar
  230. Wang G, Post WM, Mayes MA (2013a) Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses. Ecol Appl 23:255–272PubMedCrossRefGoogle Scholar
  231. Wang Q, Burger M, Doane T, Horwath W, Castillo A, Mitloehner F (2013b) Effects of inorganic v. organic copper on denitrification in agricultural soil. Adv Anim Biosci 4:42–49CrossRefGoogle Scholar
  232. Wang G, Jagadamma S, Mayes MA, Schadt CW, Steinweg JM, Gu L, Post WM (2015) Microbial dormancy improves development and experimental validation of ecosystem model. ISME J 9:226–237PubMedCrossRefGoogle Scholar
  233. Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056PubMedPubMedCentralCrossRefGoogle Scholar
  234. Waring BG, Averill C, Hawkes CV (2013) Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecol Lett 16:887–894PubMedCrossRefGoogle Scholar
  235. Weber CF, Zak DR, Hungate BA, Jackson RB, Vilgalys R, Evans RD, Schadt CW, Megonigal JP, Kuske CR (2011) Responses of soil cellulolytic fungal communities to elevated atmospheric CO2 are complex and variable across five ecosystems. Environ Microbiol 13:2778–2793PubMedCrossRefGoogle Scholar
  236. Wei H, Guenet B, Vicca S, Nunan N, AbdElgawad H, Pouteau V, Shen W, Janssens IA (2014) Thermal acclimation of organic matter decomposition in an artificial forest soil is related to shifts in microbial community structure. Soil Biol Biochem 71:1–12CrossRefGoogle Scholar
  237. Wieder WR, Bonan GB, Allison SD (2013) Global soil carbon projections are improved by modelling microbial processes. Nat Clim Chang 3:909–912CrossRefGoogle Scholar
  238. Wieder W, Grandy A, Kallenbach C, Bonan G (2014) Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model. Biogeosciences 11:3899–3917CrossRefGoogle Scholar
  239. Wieder WR, Allison SD, Davidson EA, Georgiou K, Hararuk O, He Y, Hopkins F, Luo Y, Smith MJ, Sulman B (2015) Explicitly representing soil microbial processes in Earth system models. Glob Biogeochem Cycles 29:1782–1800CrossRefGoogle Scholar
  240. Xu X, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749CrossRefGoogle Scholar
  241. 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 17:547–555PubMedCrossRefGoogle Scholar
  242. Xu X, Elias DA, Graham DE, Phelps TJ, Carrol SL, Wullschleger SD, Thornton PE (2015) A microbial functional group based module for simulating methane production and consumption: application to an incubation permafrost soil. J Geophys Res Biogeosci 120:1315–1333CrossRefGoogle Scholar
  243. Xu X, Schimel JP, Janssens IA, Song X, Song C, Yu G, Sinsabaugh RL, Tang D, Zhang X, Thornton PE (2017) Global pattern and controls of soil microbial metabolic quotient. Ecol Monogr 87(3):429–441CrossRefGoogle Scholar
  244. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645PubMedCrossRefGoogle Scholar
  245. Youssef NH, Couger M, McCully AL, Criado AEG, Elshahed MS (2015) Assessing the global phylum level diversity within the bacterial domain: a review. J Adv Res 6:269–282PubMedCrossRefGoogle Scholar
  246. Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–155CrossRefGoogle Scholar
  247. Zona D, Gioli B, Commane R, Lindaas J, Wofsy SC, Miller CE, Dinardo SJ, Dengel S, Sweeney C, Karion A (2016) Cold season emissions dominate the Arctic tundra methane budget. Proc Natl Acad Sci USA 113:40–45PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.San Diego State UniversitySan DiegoUSA

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