Skip to main content

Advertisement

Log in

A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

As the earth system changes in response to human activities, a critical objective is to predict how biogeochemical process rates (e.g. nitrification, decomposition) and ecosystem function (e.g. net ecosystem productivity) will change under future conditions. A particular challenge is that the microbial communities that drive many of these processes are capable of adapting to environmental change in ways that alter ecosystem functioning. Despite evidence that microbes can adapt to temperature, precipitation regimes, and redox fluctuations, microbial communities are typically not optimally adapted to their local environment. For example, temperature optima for growth and enzyme activity are often greater than in situ temperatures in their environment. Here we discuss fundamental constraints on microbial adaptation and suggest specific environments where microbial adaptation to climate change (or lack thereof) is most likely to alter ecosystem functioning. Our framework is based on two principal assumptions. First, there are fundamental ecological trade-offs in microbial community traits that occur across environmental gradients (in time and space). These trade-offs result in shifting of microbial function (e.g. ability to take up resources at low temperature) in response to adaptation of another trait (e.g. limiting maintenance respiration at high temperature). Second, the mechanism and level of microbial community adaptation to changing environmental parameters is a function of the potential rate of change in community composition relative to the rate of environmental change. Together, this framework provides a basis for developing testable predictions about how the rate and degree of microbial adaptation to climate change will alter biogeochemical processes in aquatic and terrestrial ecosystems across the planet.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams HE, Crump BC, Kling GW (2010) Temperature controls on aquatic bacterial production and community dynamics in Arctic lakes and streams. Environ Microbiol 12(5):1319–1333

    Article  Google Scholar 

  • Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50(330):29–37

    Article  Google Scholar 

  • Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519

    Article  Google Scholar 

  • Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3(5):336–340

    Article  Google Scholar 

  • Balser TC, Wixon DL (2009) Investigating biological control over soil carbon temperature sensitivity. Glob Change Biol 15(12):2935–2949

    Article  Google Scholar 

  • Bennett AF, Lenski RE (2007) Colloquium papers: an experimental test of evolutionary trade-offs during temperature adaptation. Proc Natl Acad Sci USA 104(Suppl 1):8649–8654

    Article  Google Scholar 

  • Bergwall C, Bengtsson G (1999) Phenotypic plasticity in groundwater denitrifiers. Oikos 87(1):123–128

    Article  Google Scholar 

  • 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(12):1316–1327

    Article  Google Scholar 

  • Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12(11):2998–3006

    Article  Google Scholar 

  • Cooper VS, Bennett AF, Lenski RE (2001) Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment. Evolution 55(5):889–896

    Article  Google Scholar 

  • Crump BC, Hobbie JE (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50(6):1718–1729

    Article  Google Scholar 

  • Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation—genetics and physiology. Annu Rev Microbiol 45:569–606

    Article  Google Scholar 

  • Dai A, Trenberth KE (2004) The diurnal cycle and its depiction in the community climate system model. J Clim 17(5):930–951

    Article  Google Scholar 

  • Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440(7081):165

    Article  Google Scholar 

  • DeAngelis KM, Silver WL, Thompson AW, Firestone MK (2010) Microbial communities acclimate to recurring changes in soil redox potential status. Environ Microbiol 12(12):3137–3149

    Article  Google Scholar 

  • Del Giorgio PA, Cole JJ (2000) Bacterial energetics and growth efficiency. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New York, pp 289–325

    Google Scholar 

  • Dessureault-Rompre J, Zebarth BJ, Georgallas A, Burton DL, Grant CA, Drury CF (2010) Temperature dependence of soil nitrogen mineralization rate: comparison of mathematical models, reference temperatures and origin of the soils. Geoderma 157(3–4):97–108

    Article  Google Scholar 

  • Evans SE, Wallenstein MD (2011) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry. doi:10.1007/s10533-011-9638-3

  • Firestone MK, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere. Life sciences research report. Wiley and Sons, Chichester, pp 7–21

  • Fissore C, Giardina CP, Swanston CW, King GM, Kolka RK (2009) Variable temperature sensitivity of soil organic carbon in North American forests. Glob Change Biol 15(9):2295–2310

    Article  Google Scholar 

  • Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103(35):13104–13109

    Article  Google Scholar 

  • Gallardo A, Schlesinger WH (1992) Carbon and nitrogen limitations of soil microbial biomass in desert ecosystems. Biogeochemistry 18(1):1–17

    Article  Google Scholar 

  • Giardina CP, Ryan MG (2000) Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404(6780):858–861

    Article  Google Scholar 

  • Gonzalez JM, Sherr EB, Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl Environ Microbiol 56(3):583

    Google Scholar 

  • Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320(5879):1039–1043

    Article  Google Scholar 

  • Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature-controlled organic carbon mineralization in lake sediments. Nature 466(7305):478–481

    Google Scholar 

  • Hall EK, Neuhauser C, Cotner JB (2008) Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. ISME J 2:471–481

    Google Scholar 

  • Hall EK, Dzialowski AR, Stoxen SM, Cotner JB (2009) The effect of temperature on the coupling between phosphorus and growth in lacustrine bacterioplankton communities. Limnol Oceanogr 54(3):880–889

    Article  Google Scholar 

  • Hall EK, Singer GA, Kainz MJ, Lennon JT (2010) Evidence for a temperature acclimation mechanism in bacteria: an empirical test of a membrane-mediated trade-off. Funct Ecol 24(4):898–908

    Article  Google Scholar 

  • Hall EK, Maixner F, Franklin O, Daims H, Richter A, Battin T (2011) Linking microbial and ecosystem ecology using ecological stoichiometry: a synthesis of conceptual and empirical approaches. Ecosystems 14(2):261–273

    Article  Google Scholar 

  • Hansen J, Sato M, Ruedy R (1995) Long-term changes of the diurnal temperature cycle: implications about mechanisms of global climate change. Atmos Res 37(1–3):175–209

    Article  Google Scholar 

  • Hartley IP, Hopkins DW, Garnett MH, Sommerkorn M, Wookey PA (2008) Soil microbial respiration in arctic soil does not acclimate to temperature. Ecol Lett 11(10):1092–1100

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Hullar MAJ, Kaplan LA, Stahl DA (2006) Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72(1):713–722

    Article  Google Scholar 

  • Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW (2006) Niche partitioning among prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311(5768):1737–1740

    Article  Google Scholar 

  • 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(3):430–440

    Google Scholar 

  • Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7(1):69–80

    Article  Google Scholar 

  • Knies JL, Izem R, Supler KL, Kingsolver JG, Burch CL (2006) The genetic basis of thermal reaction norm evolution in lab and natural phage populations. PLoS Biol 4(7):e201

    Article  Google Scholar 

  • Kritzberg E, Duarte C, Wassmann P (2010) Changes in Arctic marine bacterial carbon metabolism in response to increasing temperature. Polar Biology 33(12):1673–1682

    Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(15):5111–5120

    Article  Google Scholar 

  • Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16(5):545–556

    Article  Google Scholar 

  • Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7(7):601–613

    Article  Google Scholar 

  • Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9(2):119–130

    Article  Google Scholar 

  • Lipson D, Monson R, Schmidt S, Weintraub M (2008) 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 95:23–35

    Google Scholar 

  • Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639

    Article  Google Scholar 

  • Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10(12):1170–1181

    Article  Google Scholar 

  • Liu Z, Fu B, Zheng X, Liu G (2010) Plant biomass, soil water content and soil N:P ratio regulating soil microbial functional diversity in a temperate steppe: a regional scale study. Soil Biol Biochem 42(3):445–450

    Article  Google Scholar 

  • McGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42(4):529–535

    Article  Google Scholar 

  • Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298(5601):2173–2176

    Article  Google Scholar 

  • Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76(2):151–174

    Article  Google Scholar 

  • Pena MI, Davlieva M, Bennett MR, Olson JS, Shamoo Y (2010) Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection. Mol Syst Biol 6:387. doi:10.1038/msb.2010.43

    Google Scholar 

  • Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3(7):537–546

    Article  Google Scholar 

  • Pett-Ridge J, Firestone MK (2005) Redox fluctuation structures microbial communities in a wet tropical soil. Appl Environ Microbiol 71(11):6998–7007

    Article  Google Scholar 

  • Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292(5516):504–507

    Article  Google Scholar 

  • Philippot L, Cregut M, ChËneby D, Bressan M, Dequiet S, Martin-Laurent F, Ranjard L, Lemanceau P (2008) Effect of primary mild stresses on resilience and resistance of the nitrate reducer community to a subsequent severe stress. FEMS Microbiol Lett 285(1):51–57

    Article  Google Scholar 

  • Portner HO, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79(2):295–313

    Article  Google Scholar 

  • Rensing C, Newby DT, Pepper I (2002) The role of selective pressure and selfish DNA in horizontal gene transfer and soil microbial community adaptation. Soil Biol Biochem 34(3):285–296

    Article  Google Scholar 

  • Riehle MM, Bennett AF, Long AD (2001) Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci USA 98(2):525–530

    Article  Google Scholar 

  • Rinnan R, Rousk J, Yergeau E, Kowalchuk GA, Baath E (2009) Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming. Glob Change Biol 15(11):2615–2625

    Article  Google Scholar 

  • Rivkin RB, Anderson MR, Lajzerowicz C (1996) Microbial processes in cold oceans. 1. Relationship between temperature and bacterial growth rate. Aquat Microb Ecol 10(3):243–254

    Article  Google Scholar 

  • Roessler M, Muller V (2001) Osmoadaptation in bacteria and archaea: common principles and differences. Environ Microbiol 3(12):743–754

    Article  Google Scholar 

  • Rose MR, Lauder GV (1996) Adaptation. Academic Press, San Diego

    Google Scholar 

  • Rousk J, Brookes PC, Baath E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75(6):1589–1596

    Article  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394

    Article  Google Scholar 

  • Shade A, Kent AD, Jones SE, Newton RJ, Triplett EW, McMahon KD (2007) Interannual dynamics and phenology of bacterial communities in a eutrophic lake. Limnol Oceanogr 52(2):487–494

    Article  Google Scholar 

  • Simon M, Gloeckner FO, Amann R (1999) Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean. Aquat Microb Ecol 18(3):275–284

    Article  Google Scholar 

  • Sleator RD, Hill C (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26(1):49–71

    Article  Google Scholar 

  • Stres B, Danevčič T, Pal L, Fuka MM, Resman L, Leskovec S, Hacin J, Stopar D, Mahne I, Mandic-Mulec I (2008) Influence of temperature and soil water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiol Ecol 66(1):110–122

    Article  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90(2):441–451

    Article  Google Scholar 

  • Szukics U, Abell GCJ, Hödl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72(3):395–406

    Article  Google Scholar 

  • Taylor PG, Townsend AR (2010) Stoichiometric control of organic carbon–nitrate relationships from soils to the sea. Nature 464(7292):1178–1181

    Article  Google Scholar 

  • Tobor-Kaplon MA, Bloem J, De Ruiter PC (2006) Functional stability of microbial communities from long-term stressed soils to additional disturbance. Environ Toxicol Chem 25(8):1993–1999

    Article  Google Scholar 

  • Treseder KK, Balser TC, Bradford MA, Brodie EL, Dubinsky EA, Eviner VT, Hofmockel KS, Lennon JT, Levine UY, MacGregor BJ, Pett-Ridge J, Waldrop MP (2011) Integrating microbial ecology into ecosystem models: challenges and priorities. Biogeochemistry. doi:10.1007/s10533-011-9636-5

  • Trevors JT, Barkay T, Bourquin AW (1987) Gene transfer among bacteria in soil and aquatic environments: a review. Can J Microbiol 33(3):191–198

    Article  Google Scholar 

  • Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD (2011) A framework for representing microbial decomposition in coupled climate models. Biogeochemistry. doi:10.1007/s10533-011-9635-6

  • Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna J-M, Schwenk K, Zwart G, Degans H, Vyverman W, De Meester L (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc Natl Acad Sci USA 104(51):20404–20409

    Article  Google Scholar 

  • Van Mooy BAS, Rocap G, Fredricks HF, Evans CT, Devol AH (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103(23):8607–8612

    Article  Google Scholar 

  • Vicca S, Fivez L, Kockelbergh F, Van Pelt D, Segers JJR, Meire P, Ceulemans R, Janssens IA (2009) No signs of thermal acclimation of heterotrophic respiration from peat soils exposed to different water levels. Soil Biol Biochem 41(9):2014–2016

    Article  Google Scholar 

  • Waldrop MP, Firestone MK (2006) Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb Ecol 52(3):470–479

    Article  Google Scholar 

  • Wallenstein MD, Hess AM, Lewis MR, Steltzer H, Ayres E (2010a) Decomposition of aspen leaf litter results in unique metabolomes when decomposed under different tree species. Soil Biol Biochem 42(3):484–490

    Article  Google Scholar 

  • Wallenstein MD, Steinweg JM, Ernakovich J, Allison S, Sinsabaugh RL (2010b) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates. In: Shukla G, Varma A (eds) Soil enzymology. Soil biology series. Springer, New York

    Google Scholar 

  • Webb CT, Hoeting JA, Ames GM, Pyne MI, Poff NL (2010) A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecol Lett 13(3):267–283

    Article  Google Scholar 

  • Wilson JM, Griffin DM (1975) Water potential and the respiration of microorganisms in the soil. Soil Biol Biochem 7(3):199–204

    Article  Google Scholar 

  • Young IM, Crawford JW, Nunan N, Otten W, Spiers A (2008) Chapter 4 Microbial distribution in soils: physics and scaling. In: Donald LS (ed) Advances in Agronomy. Academic Press, pp 81–121

  • Zogg GP, Zak DR, Ringelberg DB, MacDonald NW, Pregitzer KS, White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61(2):475–481

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by grants to MDW from the National Science Foundation Division of Environmental Biology (#1020540 and 0842315) and Office of Polar Programs (#0902030 and 0733074).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthew D. Wallenstein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wallenstein, M.D., Hall, E.K. A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109, 35–47 (2012). https://doi.org/10.1007/s10533-011-9641-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-011-9641-8

Keywords

Navigation