Earth’s climate is warming, and there is evidence that increased temperature alters soil C cycling, which may result in a self-reinforcing (positive), microbial mediated feedback to the climate system. Though soil microbes are major drivers of soil C cycling, we lack an understanding of how temperature affects SOM decomposition. Numerous studies have explored, to differing degrees, the extent to which climate change may affect biodiversity. While there is ample evidence that community diversity begets ecosystem stability and resilience, we know of keystone species that perform functions whose effects far outweigh their relative abundance. In this paper, we first review the meaning of microbial diversity and how it relates to ecosystem function, then conduct a literature review of field-based climate warming studies that have made some measure of microbial diversity. Finally, we explore how measures of diversity may yield a larger, more complete picture of climate warming effects on microbial communities, and how this may translate to altered carbon cycling and greenhouse gas emissions. While warming effects seem to be ecosystem-specific, the lack of observable consistency between measures is due in some part to the diversity in measures of microbial diversity.
References
[1]
Davidson, E.A.; Janssens, I.A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006, 440, 165–173, doi:10.1038/nature04514.
[2]
Schlesinger, W.H.; Andrews, J.A. Soil respiration and the global carbon cycle. Biogeochemistry 2000, 48, 7–20, doi:10.1023/A:1006247623877.
[3]
Conrad, R. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol. Rev. 1996, 60, 609–640.
[4]
Falkowski, P.G.; Fenchel, T.; Delong, E.F. The Microbial Engines That Drive Earth’s Biogeochemical Cycles. Science 2008, 320, 1034–1039, doi:10.1126/science.1153213.
[5]
Canadell, J.G.; Quéré, C.L.; Raupach, M.R.; Field, C.B.; Buitenhuis, E.T.; Ciais, P.; Conway, T.J.; Gillett, N.P.; Houghton, R.A.; Marland, G. Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proc. Natl. Acad. Sci. USA 2007, 104, 18866–18870, doi:10.1073/pnas.0702737104.
[6]
Frey, S.D.; Drijber, R.; Smith, H.; Melillo, J. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol. Biochem. 2008, 40, 2904–2907, doi:10.1016/j.soilbio.2008.07.020.
Frey, S.D.; Lee, J.; Melillo, J.M.; Six, J. Soil carbon cycling: the temperature response of microbial efficiency and its feedback to climate. Nat. Clim. Change 2013, 3, 395–398.
Reid, A. Incorporating Microbial Processes into Climate Change Models. Available online: http://academy.asm.org/images/stories/documents/Incorporating_Microbial_Processes_Into_Climate_Models.pdf (accessed on 15 April 2013).
[11]
Melillo, J.M.; Steudler, P.A.; Aber, J.D.; Newkirk, K.M.; Lux, H.; Bowles, F.P.; Catricala, C.; Magill, A.H.; Ahrens, T.; Morrisseau, S. Soil Warming and Carbon-Cycle Feedbacks to the Climate System. Science 2002, 298, 2173–2176, doi:10.1126/science.1074153.
[12]
Melillo, J.M.; Butler, S.; Johnson, J.; Mohan, J.; Steudler, P.; Lux, H.; Burrows, E.; Bowles, F.; Smith, R.; Scott, L.; et al. Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proc. Natl. Acad. Sci. USA 2011, 108, 9508–9512, doi:10.1073/pnas.1018189108.
[13]
Loreau, M.; Naeem, S.; Inchausti, P.; Bengtsson, J.; Grime, J.P.; Hector, A.; Hooper, D.U.; Huston, M.A.; Raffaelli, D.; Schmid, B.; et al. Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges. Science 2001, 294, 804–808, doi:10.1126/science.1064088.
[14]
Ptacnik, R.; Solimini, A.G.; Andersen, T.; Tamminen, T.; Brettum, P.; Lepist?, L.; Willén, E.; Rekolainen, S. Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proc. Natl. Acad. Sci. USA 2008, 105, 5134–5138, doi:10.1073/pnas.0708328105.
[15]
Shade, A.; Peter, H.; Allison, S.D.; Baho, D.L.; Berga, M.; Bürgmann, H.; Huber, D.H.; Lennon, J.T.; Martiny, J.B.H.; Matulich, K.L.; et al. Fundamentals of microbial community resistance and resilience. Front. Aquat. Microbiol. 2012, 3, 417.
[16]
Gilbert, J.A.; Field, D.; Swift, P.; Thomas, S.; Cummings, D.; Temperton, B.; Weynberg, K.; Huse, S.; Hughes, M.; Joint, I.; et al. The Taxonomic and Functional Diversity of Microbes at a Temperate Coastal Site: A “Multi-Omic” Study of Seasonal and Diel Temporal Variation. PloS. One 2010, 5, e15545, doi:10.1371/journal.pone.0015545.
[17]
Martiny, A.C.; Treseder, K.; Pusch, G. Phylogenetic conservatism of functional traits in microorganisms. Isme. J. 2013, 7, 830–838, doi:10.1038/ismej.2012.160.
[18]
Tilman, D.; Reich, P.B.; Knops, J.; Wedin, D.; Mielke, T.; Lehman, C. Diversity and Productivity in a Long-Term Grassland Experiment. Science 2001, 294, 843–845, doi:10.1126/science.1060391.
[19]
Tilman, D.; Downing, J.A. Biodiversity and stability in grasslands. Nature 1994, 367, 363–365, doi:10.1038/367363a0.
[20]
Van Elsas, J.D.; Chiurazzi, M.; Mallon, C.A.; Elhottovā, D.; Kri?t?fek, V.; Salles, J.F. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl. Acad. Sci. USA. 2012, 109, 1159–1164.
Fierer, N.; Lennon, J.T. The generation and maintenance of diversity in microbial communities. Am. J. Bot. 2011, 98, 439–448, doi:10.3732/ajb.1000498.
[23]
Lennon, J.T.; Aanderud, Z.T.; Lehmkuhl, B.K.; Schoolmaster, D.R., Jr. Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 2012, 93, 1867–1879, doi:10.1890/11-1745.1.
[24]
Crowther, T.W.; Bradford, M.A. Thermal acclimation in widespread heterotrophic soil microbes. Ecol. Lett. 2013, 16, 469–477, doi:10.1111/ele.12069.
[25]
Rosenfeld, J.S. Functional redundancy in ecology and conservation. OIkos 2002, 98, 156–162, doi:10.1034/j.1600-0706.2002.980116.x.
[26]
Schimel, J.; Balser, T.C.; Wallenstein, M. Microbial stress-responses physiology and its implications for ecosystem function. Ecology 2007, 88, 1386–1394, doi:10.1890/06-0219.
[27]
Rillig, M.C.; Wright, S.F.; Shaw, M.R.; Field, C.B. Artificial Climate Warming Positively Affects Arbuscular Mycorrhizae but Decreases Soil Aggregate Water Stability in an Annual Grassland. Oikos 2002, 97, 52–58, doi:10.1034/j.1600-0706.2002.970105.x.
[28]
Girvan, M.S.; Campbell, C.D.; Killham, K.; Prosser, J.I.; Glover, L.A. Bacterial diversity promotes community stability and functional resilience after perturbation. Environ. Microbiol. 2005, 7, 301–313, doi:10.1111/j.1462-2920.2005.00695.x.
[29]
Hol, W.H.G.; de Boer, W.; Termorshuizen, A.J.; Meyer, K.M.; Schneider, J.H. M.; van Dam, N.M.; van Veen, J.A.; van der Putten, W.H. Reduction of rare soil microbes modifies plant–herbivore interactions. Ecol. Lett. 2010, 13, 292–301, doi:10.1111/j.1461-0248.2009.01424.x.
[30]
Wertz, S.; Degrange, V.; Prosser, J.I.; Poly, F.; Commeaux, C.; Guillaumaud, N.; le Roux, X. Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ. Microbiol. 2007, 9, 2211–2219, doi:10.1111/j.1462-2920.2007.01335.x.
[31]
Nielsen, U.; Ayres, E.; Wall, D.; Bardgett, R. Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur. J. Soil Sci. 2011.
[32]
Tyson, G.W.; Chapman, J.; Hugenholtz, P.; Allen, E.E.; Ram, R.J.; Richardson, P.M.; Solovyev, V.V.; Rubin, E.M.; Rokhsar, D.S.; Banfield, J.F. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 2004, 428, 37–43, doi:10.1038/nature02340.
[33]
Kato, S.; Haruta, S.; Cui, Z.J.; Ishii, M.; Igarashi, Y. Effective cellulose degradation by a mixed-culture system composed of a cellulolytic Clostridium and aerobic non-cellulolytic bacteria. Fems. Microbiol. Ecol. 2004, 51, 133–142.
[34]
Pester, M.; Bittner, N.; Deevong, P.; Wagner, M.; Loy, A. A “rare biosphere”microorganism contributes to sulfate reduction in a peatland. Isme. J. 2010, 4, 1591–1602, doi:10.1038/ismej.2010.75.
[35]
Fierer, N.; Jackson, R.B. The Diversity and Biogeography of Soil Bacterial Communities. Proc. Natl. Acad. Sci. USA. 2006, 103, 626–631, doi:10.1073/pnas.0507535103.
[36]
Lozupone, C.A.; Knight, R. Global patterns in bacterial diversity. Proc. Natl. Acad. Sci.USA 2007, 104, 11436, doi:10.1073/pnas.0611525104.
[37]
Lauber, C.L.; Hamady, M.; Knight, R.; Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 2009, 75, 5111–5120, doi:10.1128/AEM.00335-09.
[38]
Philippot, L.; Andersson, S.G.E.; Battin, T.J.; Prosser, J.I.; Schimel, J.P.; Whitman, W.B.; Hallin, S. The ecological coherence of high bacterial taxonomic ranks. Nat. Rev. Microbiol. 2010, 8, 523–529, doi:10.1038/nrmicro2367.
[39]
Fierer, N.; Lauber, C.L.; Ramirez, K.S.; Zaneveld, J.; Bradford, M.A.; Knight, R. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. Isme. J. 2012, 6, 1007–1017, doi:10.1038/ismej.2011.159.
Schindlbacher, A.; Rodler, A.; Kuffner, M.; Kitzler, B.; Sessitsch, A.; Zechmeister-Boltenstern, S. Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol. Biochem. 2011, 43, 1417–1425, doi:10.1016/j.soilbio.2011.03.005.
[48]
Allison, S.D.; Treseder, K.K. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biol. 2008, 14, 2898–2909, doi:10.1111/j.1365-2486.2008.01716.x.
[49]
Allison, S.D.; McGuire, K.L.; Treseder, K.K. Resistance of microbial and soil properties to warming treatment seven years after boreal fire. Soil Biol. Biochem. 2010, 42, 1872–1878, doi:10.1016/j.soilbio.2010.07.011.
[50]
NOAA Climate Data Online (CDO)-COOP: 502339. Available online: http://www.ncdc.noaa.gov/cdo-web/confirmation/ (accessed on 15 April 2013).
[51]
Dorrepaal, E.; Toet, S.; van Logtestijn, R.S.P.; Swart, E.; van de Weg, M.J.; Callaghan, T.V.; Aerts, R. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 2009, 460, 616–619, doi:10.1038/nature08216.
[52]
Weedon, J.T.; Kowalchuk, G.A.; Aerts, R.; van Hal, J.; van Logtestijn, R.; Ta?, N.; R?ling, W.; van Bodegom, P.M. Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Global Change Biol. 2012, 18, 138–150, doi:10.1111/j.1365-2486.2011.02548.x.
[53]
Rinnan, R.; Michelsen, A.; B??th, E.; Jonasson, S. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Global Change Biol. 2007, 13, 28–39, doi:10.1111/j.1365-2486.2006.01263.x.
[54]
Bokhorst, S.; Huiskes, A.; Convey, P.; Aerts, R. The effect of environmental change on vascular plant and cryptogam communities from the Falkland Islands and the Maritime Antarctic. Bmc. Ecol. 2007, 7, 15, doi:10.1186/1472-6785-7-15.
[55]
Bokhorst, S.; Huiskes, A.; Convey, P.; Aerts, R. External nutrient inputs into terrestrial ecosystems of the Falkland Islands and the Maritime Antarctic region. Polar Biol. 2007, 30, 1315–1321, doi:10.1007/s00300-007-0292-0.
[56]
Yergeau, E.; Bokhorst, S.; Kang, S.; Zhou, J.; Greer, C.W.; Aerts, R.; Kowalchuk, G.A. Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. Isme. J. 2012, 6, 692–702, doi:10.1038/ismej.2011.124.
[57]
Rustad, L.E.; Campbell, J.L.; Marion, G.M.; Norby, R.J.; Mitchell, M.J.; Hartley, A.E.; Cornelissen, J.H.C.; Gurevitch, J. Gcte-News A Meta-Analysis of the Response of Soil Respiration, Net Nitrogen Mineralization, and Aboveground Plant Growth to Experimental Ecosystem Warming. Oecologia 2001, 126, 543–562, doi:10.1007/s004420000544.
[58]
Wu, Z.; Dijkstra, P.; Koch, G.W.; Pe?uelas, J.; Hungate, B.A. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biol. 2011, 17, 927–942, doi:10.1111/j.1365-2486.2010.02302.x.
[59]
Zogg, G.P.; Zak, D.R.; Ringelberg, D.B.; White, D.C.; MacDonald, N.W.; Pregitzer, K.S. Compositional and Functional Shifts in Microbial Communities Due to Soil Warming. Soil Sci. Soc. Am. J. 1997, 61, 475–481, doi:10.2136/sssaj1997.03615995006100020015x.
[60]
Blankinship, J.; Niklaus, P.; Hungate, B. A meta-analysis of responses of soil biota to global change. Oecologia 2011, 165, 553–565, doi:10.1007/s00442-011-1909-0.
[61]
Andrews, J.A.; Matamala, R.; Westover, K.M.; Schlesinger, W.H. Temperature effects on the diversity of soil heterotrophs and the δ13C of soil-respired CO2. Soil Biol. Biochem. 2000, 32, 699–706, doi:10.1016/S0038-0717(99)00206-0.
[62]
Pettersson, M.; B??th, E. Temperature-dependent changes in the soil bacterial community in limed and unlimed soil. Fems. Microbiol. Ecol. 2003, 45, 13–21, doi:10.1016/S0168-6496(03)00106-5.
[63]
The Core Writing Team. Climate Change 2007: Synthesis Report Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; IPCC: Geneva, Sweden, 2007; p. 104.
[64]
Jonasson, S.; Michelsen, A.; Schmidt, I.K.; Nielsen, E.V. Responses in microbes and platns to changed temperature, nutrient, and light regimes in the Arctic. Ecology 1999, 80, 1828–1843, doi:10.1890/0012-9658(1999)080[1828:RIMAPT]2.0.CO;2.
[65]
Foster, D.R.; Colburn, E.; Crone, E.; Ellison, A.; Hart, C.; Lambert, K.; Orwig, D.; Pallant, J.; Snow, P.; Stinson, K.; et al. New Science, Synthesis, Scholarship, and Strategic Vision for Society-HF LTER V 2012–2018. 2012. Available online: http://harvardforest.fas.harvard.edu/sites/harvardforest.fas.harvard.edu/files/publications/pdfs/LTERV-2012-proposal.pdf (accessed on 15 April 2013).
[66]
Wardle, D.A.; Bardgett, R.D.; Klironomos, J.N.; Set?l?, H.; van der Putten, W.H.; Wall, D.H. Ecological linkages between aboveground and belowground biota. Science 2004, 304, 1629, doi:10.1126/science.1094875.
[67]
Conant, R.T.; Ryan, M.G.; ?gren, G.I.; Birge, H.E.; Davidson, E.A.; Eliasson, P.E.; Evans, S.E.; Frey, S.D.; Giardina, C.P.; Hopkins, F.M.; et al. Temperature and soil organic matter decomposition rates–synthesis of current knowledge and a way forward. Global Change Biol. 2011, 17, 3392–3404, doi:10.1111/j.1365-2486.2011.02496.x.
[68]
Schurig, C.; Smittenberg, R.H.; Berger, J.; Kraft, F.; Woche, S.; Goebel, M.-O.; Heipieper, H.J.; Miltner, A.; Kaestner, M. Microbial cell-envelope fragments and the formation of soil organic matter: a case study from a glacier forefield. Biogeochemistry 2013, 113, 595–612, doi:10.1007/s10533-012-9791-3.
[69]
Cotrufo, M.F.; Wallenstein, M.D.; Boot, C.M.; Denef, K.; Paul, E. The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: Do labile plant inputs form stable soil organic matter? Global Change Biol 2013, 19, 988–995.
[70]
Fierer, N.; Bradford, M.A.; Jackson, R.B. Toward an ecological classification of soil bacteria. Ecology 2007, 88, 1354–1364, doi:10.1890/05-1839.
[71]
Schindlbacher, A.; Zechmeister-Boltenstern, S.; Jandl, R. Carbon losses due to soil warming: Do autotrophic and heterotrophic soil respiration respond equally? Global Change Biol 2009, 15, 901–913.
[72]
Manzoni, S.; Taylor, P.; Richter, A.; Porporato, A.; ?gren, G.I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 2012, 196, 79–91, doi:10.1111/j.1469-8137.2012.04225.x.
[73]
Suseela, V.; Conant, R.T.; Wallenstein, M.D.; Dukes, J.S. Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Global Change Biol. 2012, 18, 336–348, doi:10.1111/j.1365-2486.2011.02516.x.
[74]
Gutknecht, J.L.M.; Field, C.B.; Balser, T.C. Microbial communities and their responses to simulated global change fluctuate greatly over multiple years. Global Change Biol. 2012, 18, 2256–2269, doi:10.1111/j.1365-2486.2012.02686.x.
[75]
Nielsen, P.; Petersen, S.O. Ester-linked polar lipid fatty acid profiles of soil microbial communities: a comparison of extraction methods and evaluation of interference from humic acids. Soil Biol. Biochem. 2000, 32, 1241–1249, doi:10.1016/S0038-0717(00)00041-9.
[76]
Papadopoulou, E.S.; Karpouzas, D.G.; Menkissoglu-Spiroudi, U. Extraction Parameters Significantly Influence the Quantity and the Profile of PLFAs Extracted from Soils. Microb. Ecol. 2011, 62, 704–714, doi:10.1007/s00248-011-9863-2.
[77]
Chowdhury, T.R.; Dick, R.P. Standardizing methylation method during phospholipid fatty acid analysis to profile soil microbial communities. J. Microbiol. Methods 2012, 88, 285–291, doi:10.1016/j.mimet.2011.12.008.
[78]
Haney, R.I.; Franzluebbers, A.; Hons, F.; Zuberer, D.A. Soil C extracted with water or K2SO4: pH effect on determination of microbial biomass? Can. J. Soil Sci. 1999, 79, 529–533.
[79]
Bates, S.T.; Clemente, J.C.; Flores, G.E.; Walters, W.A.; Parfrey, L.W.; Knight, R.; Fierer, N. Global biogeography of highly diverse protistan communities in soil. Isme. J. 2013, 7, 652–659, doi:10.1038/ismej.2012.147.
[80]
Deslippe, J.R.; Egger, K.N.; Henry, G.H.R. Impacts of warming and fertilization on nitrogen-fixing microbial communities in the Canadian High Arctic. Fems. Microbiol. Ecol. 2005, 53, 41–50, doi:10.1016/j.femsec.2004.12.002.
[81]
Harte, J.; Saleska, S.; Shih, T. Shifts in plant dominance control carbon-cycle responses to experimental warming and widespread drought. Environ. Res. Lett. 2006, 1, 014001, doi:10.1088/1748-9326/1/1/014001.
[82]
Walker, M.D.; Wahren, C.H.; Hollister, R.D.; Henry, G.H.R.; Ahlquist, L.E.; Alatalo, J.M.; Bret-Harte, M.S.; Calef, M.P.; Callaghan, T.V.; Carroll, A.B.; et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl. Acad. Sci. USA 2006, 103, 1342–1346, doi:10.1073/pnas.0503198103.
[83]
Prasad, A.M.; Iverson, L.R.; Matthews, S.; Peters, M. A Climate Change Atlas for 134 Forest Tree Species of the Eastern United States, Available online: http://www.nrs.fs.fed.us/atlas/tree/ (accessed on 15 April 2013).
[84]
Hoeppner, S.S.; Dukes, J.S. Interactive responses of old-field plant growth and composition to warming and precipitation. Global Change Biol. 2012, 18, 1754–1768, doi:10.1111/j.1365-2486.2011.02626.x.
[85]
Tharayil, N.; Suseela, V.; Triebwasser, D.J.; Preston, C.M.; Gerard, P.D.; Dukes, J.S. Changes in the structural composition and reactivity of Acer rubrum leaf litter tannins exposed to warming and altered precipitation: climatic stress-induced tannins are more reactive. New Phytol. 2011, 191, 132–145, doi:10.1111/j.1469-8137.2011.03667.x.
[86]
Zhou, Y.; Tang, J.; Melillo, J.M.; Butler, S.; Mohan, J.E. Root standing crop and chemistry after six years of soil warming in a temperate forest. Tree Physiol. 2011, 31, 707–717, doi:10.1093/treephys/tpr066.
[87]
Bradford, M.A.; Watts, B.W.; Davies, C.A. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Global Change Biol. 2010, 16, 1576–1588, doi:10.1111/j.1365-2486.2009.02040.x.
[88]
Belay-Tedla, A.; Zhou, X.; Su, B.; Wan, S.; Luo, Y. Labile, recalcitrant, and microbial carbon and nitrogen pools of a tallgrass prairie soil in the US Great Plains subjected to experimental warming and clipping. Soil Biol. Biochem. 2009, 41, 110–116, doi:10.1016/j.soilbio.2008.10.003.