Trait-based approaches for understanding microbial biodiversity and ecosystem functioning

Frontiers in Microbiology

Volumn 5, Issue MAY, 2014, Pages

  Krause, Sascha ^a,b   Le Roux, Xavier ^c   Niklaus, Pascal A ^d   van Bodegom, Peter M ^e   Lennon T , Jay ^f   Bertilsson, Stefan ^g   Grossart, Hans Peter ^h,i   Philippot, Laurent ^j   Bodelier, Paul L E ^a  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b University of Washington   (United States)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e VU UNIVERSITY AMSTERDAM   (Netherlands)

^f INDIANA UNIVERSITY   (United States)

^g UPPSALA UNIVERSITY   (Sweden)

^h LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

ⁱ UNIVERSITY OF POTSDAM   (Germany)

^j UNIV BOURGOGNE FRANCHE COMTÉ   (France)

more..

Author keywords

Ecological theory; Ecosystem function; Functional traits; Microbial diversity; Study designs

Indexed keywords

RNA 16S; STABLE ISOTOPE;

BIOLOGICAL TRAIT; ECOSYSTEM; GENE SEQUENCE; GENOMICS; HORIZONTAL GENE TRANSFER; METABOLOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIAL METABOLISM; NONHUMAN; PHYLOGENY; PROTEOMICS; REVIEW; RNA GENE; TAXONOMY; TRANSCRIPTOMICS;

EID: 84903898896     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00251     Document Type: Review

References (99)

1. Abrams, P. A. (1995). Monotonic or unimodal diversity-productivity gradients: what does competition theory predict? Ecology 76, 2019-2027. doi: 10.2307/1941677
2. Allison, S. D., and Gessner, M. (2012). A trait-based approach for modelling microbial litter decomposition. Ecol. Lett. 15, 1058-1070. doi: 10.1111/j.1461-0248.2012.01807.x
3. Attard, E., Poly, F., Commeaux, C., Laurent, F., Terada, A., Smets, B. F., et al. (2010). Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environ. Microbiol. 12, 315-326. doi: 10.1111/j.1462-2920.2009.02070.x
4. Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J. S., Nakashizuka, T., Raffaelli, D., et al. (2006). Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146-1156. doi: 10.1111/j.1461-0248.2006.00963.x
5. Barberan, A., Fernandez-Guerra, A., Bohannan, B. J. M., and Casamayor, E. O. (2012). Exploration of community traits as ecological markers in microbial metagenomes. Mol. Ecol. 21, 1909-1917. doi: 10.1111/j.1365-294X.2011.05383.x
6. Bayjanov, J. R., Molenaar, D., Tzeneva, V., Siezen, R. J., and Van Hijum, S. A. (2012). PhenoLink-a web-tool for linking phenotype to ~omics data for bacteria: application to gene-trait matching for Lactobacillus plantarum strains. BMC Genomics 13:170. doi: 10.1186/1471-2164-13-170
7. Begon, M., Townsend, C. R., and Harper, J. L. (2006). ECOLOGY: From Individuals to Ecosystems. Malden: Blackwell Publishing.
8. Behrens, S., Kappler, A., and Obst, M. (2012). Linking environmental processes to the in situ functioning of microorganisms by high-resolution secondary ion mass spectrometry (NanoSIMS) and scanning transmission X-ray microscopy (STXM). Environ. Microbiol. 14, 2851-2869. doi: 10.1111/j.1462-2920.2012.02724.x
9. Bell, T., Newman, J. A., Silverman, B. W., Turner, S. L., and Lilley, A. K. (2005). The contribution of species richness and composition to bacterial services. Nature 436, 1157-1160. doi: 10.1038/nature03891
10. Blagodatskaya, E., and Kuzyakov, Y. (2013). Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol. Biochem. 67, 192-211. doi: 10.1016/j.soilbio.2013.08.024
11. Bodelier, P. L. E., Meima-Franke, M., Hordijk, C. A., Steenbergh, A. K., Hefting, M. M., Bodrossy, L., et al. (2013). Microbial minorities modulate methane consumption through niche partitioning. ISME J. 7, 2214-2228. doi: 10.1038/ismej.2013.99
12. Bouskill, N., Tang, J., Riley, W. J., and Brodie, E. L. (2012). Trait-based representation of biological nitrification: model development, testing, and predicted community composition. Front. Microbiol. 3:364. doi: 10.3389/fmicb.2012.00364
13. Brovkin, V., Van Bodegom, P. M., Kleinen, T., Wirth, C., Cornwell, W. K., Cornelissen, J. H. C., et al. (2012). Plant-driven variation in decomposition rates improves projections of global litter stock distribution. Biogeosciences 9, 565-576. doi: 10.5194/bg-9-565-2012
14. Bruno, J. F., Stachowicz, J. J., and Bertness, M. D. (2003). Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119-125. doi: 10.1016/S0169-5347(02)00045-9
15. Cadotte, M. W., Cardinale, B. J., and Oakley, T. H. (2008). Evolutionary history and the effect of biodiversity on plant productivity. Proc. Natl. Acad. Sci. U.S.A. 105, 17012-17017. doi: 10.1073/pnas.0805962105
16. Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C. A., Turnbaugh, P. J., et al. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516-4522. doi: 10.1073/pnas.1000080107
17. Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., et al. (2012). Biodiversity loss and its impact on humanity. Nature 486, 59-67. doi: 10.1038/Nature11148
18. Casey, J. R., Lomas, M. W., Mandecki, J., and Walker, D. E. (2007). Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum. Geophys. Res. Lett. 34:L10604. doi: 10.1029/2006GL028725
19. Chen, Y., Dumont, M. G., Neufeld, J. D., Bodrossy, L., Stralis-Pavese, N., McNamara, N. P., et al. (2008). Revealing the uncultivated majority: combining DNA stable-isotope probing, multiple displacement amplification and metagenomic analyses of uncultivated Methylocystis in acidic peatlands. Environ. Microbiol. 10, 2609-2622. doi: 10.1111/j.1462-2920.2008.01683.x
20. Cox, P., Wilkinson, S. P., and Anderson, J. M. (2001). Effects of fungal inocula on the decomposition of lignin and structural polysaccharides in Pinus sylvestris litter. Biol. Fert. Soils 33, 246-251. doi: 10.1007/s003740000315
21. Díaz, S., Lavorel, S., De Bello, F., Quétier, F., Grigulis, K., and Robson, T. M. (2007). Incorporating plant functional diversity effects in ecosystem service assessments. Proc. Natl. Acad. Sci. U.S.A. 104, 20684-20689. doi: 10.1073/pnas.0704716104
22. Edwards, K. F., Klausmeier, C. A., and Litchman, E. (2011). Evidence for a three-way trade-off between nitrogen and phosphorus competitive abilities and cell size in phytoplankton. Ecology 92, 2085-2095. doi: 10.1890/11-0395.1
23. Edwards, K. J., Becker, K., and Colwell, F. S. (2012). The deep, dark energy biosphere: intraterrestrial life on earth. Annu. Rev. Earth Planet. Sci. 40, 551-568. doi: 10.1146/annurev-earth-042711-105500
24. Fierer, N., Bradford, M. A., and Jackson, R. B. (2007). Toward an ecological classification of soil bacteria. Ecology 88, 1354-1364. doi: 10.1890/05-1839
25. Flynn, D. F. B., Mirotchnick, N., Jain, M., Palmer, M. I., and Naeem, S. (2011). Functional and phylogenetic diversity as predictors of biodiversity-ecosystem-function relationships. Ecology 92, 1573-1581. doi: 10.1890/10-1245.1
26. Garcia, S. L., McMahon, K. D., Martinez-Garcia, M., Srivastava, A., Sczyrba, A., Stepanauskas, R., et al. (2013). Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton. ISME J. 7, 137-147. doi: 10.1038/ismej.2012.86
27. Garland, J. L. (1996). Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol. Biochem. 28, 213-221. doi: 10.1016/0038-0717(95)00112-3
28. Ghiglione, J. F., Galand, P. E., Pommier, T., Pedros-Alio, C., Maas, E. W., Bakker, K., et al. (2012). Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc. Natl. Acad. Sci. U.S.A. 109, 17633-17638. doi: 10.1073/pnas.1208160109
29. Green, J. L., Bohannan, B. J. M., and Whitaker, R. J. (2008). Microbial biogeography: from taxonomy to traits. Science 320, 1039-1043. doi: 10.1126/science.1153475
30. Griffiths, B. S., Kuan, H. L., Ritz, K., Glover, L. A., McCaig, A. E., and Fenwick, C. (2004). The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb. Ecol. 47, 104-113. doi: 10.1007/s00248-002-2043-7
31. Griffiths, B. S., Ritz, K., Bardgett, R. D., Cook, R., Christensen, S., Ekelund, F., et al. (2000). Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship. Oikos 90, 279-294. doi: 10.1034/j.1600-0706.2000.900208.x
32. Grime, J. P. (1977). Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169-1194. doi: 10.2307/2460262
33. Haagensen, J. A., Regenberg, B., and Sternberg, C. (2011). Advanced microscopy of microbial cells. Adv. Biochem. Eng. Biotechnol. 124, 21-54. doi: 10.1007/10_2010_83
34. Hallin, S., Welsh, A., Stenstrom, J., Hallet, S., Enwall, K., Bru, D., et al. (2012). Soil functional operating range linked to microbial biodiversity and community composition using denitrifiers as model guild. PLoS ONE 7:e51962. doi: 10.1371/journal.pone.0051962
35. Hautier, Y., Niklaus, P. A., and Hector, A. (2009). Competition for light causes plant biodiversity loss after eutrophication. Science 324, 636-638. doi: 10.1126/science.1169640
36. Hedberg, P., Saetre, P., Sundberg, S., Rydin, H., and Kotowski, W. (2013). A functional trait approach to fen restoration analysis. Appl. Veg. Sci. 16, 658-666. doi: 10.1111/Avsc.12042
37. Ho, A., Kerckhof, F.-M., Luke, C., Reim, A., Krause, S., Boon, N., et al. (2013). Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ. Microbiol. Rep. 5, 335-345. doi: 10.1111/j.1758-2229.2012.00370.x
38. Hoehler, T. M., and Jorgensen, B. B. (2013). Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11, 83-94. doi: 10.1038/nrmicro2939
39. Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., et al. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3-35. doi: 10.1890/04-0922
40. Huang, W. E., Stoecker, K., Griffiths, R., Newbold, L., Daims, H., Whiteley, A. S., et al. (2007). Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 9, 1878-1889. doi: 10.1111/j.1462-2920.2007.01352.x
41. Hughes Martiny, J. B. H., Bohannan, B. J. M., Brown, J. H., Colwell, R. K., Fuhrman, J. A., Green, J. L., et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102-112. doi: 10.1038/nrmicro1341
42. Iverson, V., Morris, R. M., Frazar, C. D., Berthiaume, C. T., Morales, R. L., and Armbrust, E. V. (2012). Untangling genomes from metagenomes: revealing an uncultured class of marine euryarchaeota. Science 335, 587-590. doi: 10.1126/science.1212665
43. Janzen, R. A., Dormaar, J. F., and McGill, W. B. (1995). A community-level concept of controls on decomposition processes: decomposition of barley straw by Phanerochaete chrysosporium or Phlebia radiata in pure or mixed culture. Soil Biol. Biochem. 27, 173-179. doi: 10.1016/0038-0717(94)00164-V
44. Jones, C. M., Welsh, A., Throbäck, I. N., Dörsch, P., Bakken, L. R., and Hallin, S. (2011). Phenotypic and genotypic heterogeneity among closely related soil-borne N2- and N2O-producing Bacillus isolates harboring the nosZ gene. FEMS Microbiol. Ecol. 76, 541-552. doi: 10.1111/j.1574-6941.2011.01071.x
45. Jones, S. E., and Lennon, J. T. (2010). Dormancy contributes to the maintenance of microbial diversity. Proc. Natl. Acad. Sci. U.S.A. 107, 5881-5886. doi: 10.1073/pnas.0912765107
46. Jonsson, L. M., Nilsson, M.-C., Wardle, D. A., and Zackrisson, O. (2001). Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93, 353-364. doi: 10.1034/j.1600-0706.2001.930301.x
47. Jousset, A., Schmid, B., Scheu, S., and Eisenhauer, N. (2011). Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol. Lett. 14, 537-545. doi: 10.1111/j.1461-0248.2011.01613.x
48. Kattge, J., Díaz, S., Lavorel, S., Prentice, I. C., Leadley, P., Bönisch, G., et al. (2011). TRY-a global database of plant traits. Glob. Change Biol. 17, 2905-2935. doi: 10.1111/j.1365-2486.2011.02451.x
49. Koeppel, A., Perry, E. B., Sikorski, J., Krizanc, D., Warner, A., Ward, D. M., et al. (2008). Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc. Natl. Acad. Sci. U.S.A. 105, 2504-2509. doi: 10.1073/pnas.0712205105
50. Lavorel, S., and Garnier, E. (2002). Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol. 16, 545-556. doi: 10.1046/j.1365-2435.2002.00664.x
51. Lavorel, S., Storkey, J., Bardgett, R. D., De Bello, F., Berg, M. P., Le Roux, X., et al. (2013). A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services. J. Veg. Sci. 24, 942-948. doi: 10.1111/Jvs.12083
52. Lennon, J. T., Aanderud, Z. T., Lehmkuhl, B. K., and Schoolmaster, D. R. Jr. (2012). Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93, 1867-1879. doi: 10.1890/11-1745.1
53. Lennon, J. T., and Jones, S. E. (2011). Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 119, 119-130. doi: 10.1038/nrmicro2504
54. Le Roux, X., Recous, S., and Attard, E. (2011). "Soil microbial diversity in grasslands and its importance for grassland functioning and services," in Grassland Productivity and Ecosystem Services, eds. G. Lemaire, J. Hodgson, and A. Chabbi (Wallingford: CAB International), 158-165.
55. Le Roux, X., Schmid, B., Poly, F., Barnard, R. L., Niklaus, P. A., Guillaumaud, N., et al. (2013). Soil environmental conditions and microbial build-up mediate the effect of plant diversity on soil nitrifying and denitrifying enzyme activities in temperate grasslands. PLoS ONE 8:e61069. doi: 10.1371/journal.pone.0061069
56. Litchman, E., Klausmeier, C. A., Schofield, O. M., and Falkowski, P. G. (2007). The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol. Lett. 10, 1170-1181. doi: 10.1111/j.1461-0248.2007.01117.x
57. Loreau, M. (2000). Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91, 3-17. doi: 10.1034/j.1600-0706.2000.910101.x
58. Losos, J. B. (2008). Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett. 11, 995-1003. doi: 10.1111/j.1461-0248.2008.01229.x
59. Mackelprang, R., Waldrop, M. P., Deangelis, K. M., David, M. M., Chavarria, K. L., Blazewicz, S. J., et al. (2011). Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368-371. doi: 10.1038/Nature10576
60. Martiny, A. C., Treseder, K., and Pusch, G. (2012). Phylogenetic conservatism of functional traits in microorganisms. ISME J. 7, 830-838. doi: 10.1038/ismej.2012.160
61. Mayali, X., Weber, P. K., Brodie, E. L., Mabery, S., Hoeprich, P. D., and Pett-Ridge, J. (2012). High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use. ISME J. 6, 1210-1221. doi: 10.1038/ismej.2011.175
62. McGill, B. J., Enquist, B. J., Weiher, E., and Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178-185. doi: 10.1016/j.tree.2006.02.002
63. Nemergut, D. R., Costello, E. K., Hamady, M., Lozupone, C., Jiang, L., Schmidt, S. K., et al. (2011). Global patterns in the biogeography of bacterial taxa. Environ. Microbiol. 13, 135-144. doi: 10.1111/j.1462-2920.2010.02315.x
64. Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D., and Bertilsson, S. (2011). A guide to the natural history of freshwater lake bacteria. Microbiol. Mol. Biol. Rev. 75, 14-49. doi: 10.1128/mmbr.00028-10
65. Nielsen, J. L., Christensen, D., Kloppenborg, M., and Nielsen, P. H. (2003). Quantification of cell-specific substrate uptake by probe-defined bacteria under in situ conditions by microautoradiography and fluorescence in situ hybridization. Environ. Microbiol. 5, 202-211. doi: 10.1046/j.1462-2920.2003.00402.x
66. Norberg, J., Swaney, D. P., Dushoff, J., Lin, J., Casagrandi, R., and Levin, S. A. (2001). Phenotypic diversity and ecosystem functioning in changing environments: a theoretical framework. Proc. Natl. Acad. Sci. U.S.A. 98, 11376-11381. doi: 10.1073/pnas.171315998
67. Patra, A. K., Abbadie, L., Clays-Josserand, A., Degrange, V., Grayston, S. J., Loiseau, P., et al. (2005). Effects of grazing on microbial functional groups involved in soil N dynamics. Ecol. Monogr. 75, 65-80. doi: 10.1890/03-0837
68. Peter, H., Beier, S., Bertilsson, S., Lindstrom, E. S., Langenheder, S., and Tranvik, L. J. (2011). Function-specific response to depletion of microbial diversity. ISME J. 5, 351-361. doi: 10.1038/ismej.2010.119
69. Philippot, L., Bru, D., Saby, N. P. A., Cuhel, J., Arrouays, D., Simek, M., et al. (2009). Spatial patterns of bacterial taxa in nature reflect ecological traits of deep branches of the 16S rRNA bacterial tree. Environ. Microbiol. 11, 3096-3104. doi: 10.1111/j.1462-2920.2009.02014.x
70. Philippot, L., Spor, A., Henault, C., Bru, D., Bizouard, F., Jones, C. M., et al. (2013). Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 7, 1609-1619. doi: 10.1038/ismej.2013.34
71. Polz, M. F., Alm, E. J., and Hanage, W. P. (2013). Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29, 170-175. doi: 10.1016/j.tig.2012.12.006
72. Portillo, M. C., Leff, J. W., Lauber, C. L., and Fierer, N. (2013). Cell size distributions of soil bacterial and archaeal taxa. Appl. Environ. Microbiol. 79, 7610-7617. doi: 10.1128/aem.02710-13
73. Prosser, J. I., Bohannan, B. J. M., Curtis, T. P., Ellis, R. J., Firestone, M. K., Freckleton, R. P., et al. (2007). The role of ecological theory in microbial ecology. Nat. Rev. Microbiol. 5, 384-392. doi: 10.1038/nrmicro1643
74. Raes, J., Letunic, I., Yamada, T., Jensen, L. J., and Bork, P. (2011). Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data. Mol. Syst. Biol. 7:473. doi: 10.1038/msb.2011.6
75. Roscher, C., Schumacher, J., Gubsch, M., Lipowsky, A., Weigelt, A., Buchmann, N., et al. (2012). Using plant functional traits to explain diversity-productivity relationships. PLoS ONE 7:e36760. doi: 10.1371/journal.pone.0036760
76. Rusch, D. B., Martiny, A. C., Dupont, C. L., Halpern, A. L., and Venter, J. C. (2010). Characterization of Prochlorococcus clades from iron-depleted oceanic regions. Proc. Natl. Acad. Sci. U.S.A. 107, 16184-16189. doi: 10.1073/pnas.1009513107
77. Salles, J., Le Roux, X., and Poly, F. (2012). Relating phylogenetic and functional diversity among denitrifiers and quantifying their capacity to predict community functioning. Front. Microbiol. 3:209. doi: 10.3389/fmicb.2012.00209
78. Salles, J. F., Poly, F., Schmid, B., and Roux, X. L. (2009). Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology 90, 3324-3332. doi: 10.1890/09-0188.1
79. Schleifer, K. H. (2009). Classification of bacteria and archaea: past, present and future. Syst. Appl. Microbiol. 32, 533-542. doi: 10.1016/j.syapm.2009.09.002
80. Schmid, B. (2002). The species richness productivity controversy. Trends Ecol. Evol. 17, 113-114. doi: 10.1016/S0169-5347(01)02422-3
81. Spehn, E. M., Hector, A., Joshi, J., Scherer-Lorenzen, M., Schmid, B., Bazeley-White, E., et al. (2005). Ecosystem effects of biodiversity manipulations in European grasslands. Ecol. Monogr. 75, 37-63. doi: 10.1890/03-4101
82. Staley, J. T. (2006). The bacterial species dilemma and the genomic-phylogenetic species concept. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 361, 1899-1909. doi: 10.1098/rstb.2006.1914
83. Stepanauskas, R. (2012). Single cell genomics: an individual look at microbes. Curr.Opin. Microbiol. 15, 613-620. doi: 10.1016/j.mib.2012.09.001
84. Stiehl-Braun, P. A., Hartmann, A. A., Kandeler, E., Buchmann, N., and Niklaus, P. A. (2011). Interactive effects of drought and N fertilization on the spatial distribution of methane assimilation in grassland soils. Glob. Change Biol. 17, 2629-2639. doi: 10.1111/j.1365-2486.2011.02410.x
85. Tilman, D. (1997). The influence of functional diversity and composition on ecosystem processes. Science 277, 1300-1302. doi: 10.1126/science.277.5330.1300
86. Torsvik, V., Ovreas, L., and Thingstad, T. F. (2002). Prokaryotic diversity-Magnitude, dynamics, and controlling factors. Science 296, 1064-1066. doi: 10.1126/science.1071698
87. Treseder, K. K., Kivlin, S. N., and Hawkes, C. V. (2011). Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecol. Lett. 14, 933-938. doi: 10.1111/j.1461-0248.2011.01650.x
88. Van Der Gucht, K., Cottenie, K., Muylaert, K., Vloemans, N., Cousin, S., Declerck, S., et al. (2007). The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc. Natl. Acad. Sci. U.S.A. 104, 20404-20409. doi: 10.1073/pnas.0707200104
89. Van Der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., et al. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69-72. doi: 10.1038/23932
90. Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., et al. (2007). Let the concept of trait be functional! Oikos 116, 882-892. doi: 10.1111/j.2007.0030-1299.15559.x
91. Von Mering, C., Hugenholtz, P., Raes, J., Tringe, S. G., Doerks, T., Jensen, L. J., et al. (2007). Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315, 1126-1130. doi: 10.1126/science.1133420
92. Wallenstein, M. D., and Hall, E. K. (2012). A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109, 35-47. doi: 10.1007/s10533-011-9641-8
93. Watrous, J. D., Phelan, V. V., Hsu, C.-C., Moree, W. J., Duggan, B. M., Alexandrov, T., et al. (2013). Microbial metabolic exchange in 3D. ISME J. 7, 770-780. doi: 10.1038/ismej.2012.155
94. Webster, G., Embley, T. M., Freitag, T. E., Smith, Z., and Prosser, J. I. (2005). Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ. Microbiol. 7, 676-684. doi: 10.1111/j.1462-2920.2005.00740.x
95. Wertz, S., Degrange, V., Prosser, J. I., Poly, F., Commeaux, C., Guillaumaud, N., et al. (2007). Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ. Microbiol. 9, 2211-2219. doi: 10.1111/j.1462-2920.2007.01335.x
96. Wittebolle, L., Marzorati, M., Clement, L., Balloi, A., Daffonchio, D., Heylen, K., et al. (2009). Initial community evenness favours functionality under selective stress. Nature 458, 623-626. doi: 10.1038/nature07840
97. Wohl, D. L., Arora, S., and Gladstone, J. R. (2004). Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecology 85, 1534-1540. doi: 10.1890/03-3050
98. Wrighton, K. C., Thomas, B. C., Sharon, I., Miller, C. S., Castelle, C. J., Verberkmoes, N. C., et al. (2012). Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661-1665. doi: 10.1126/science.1224041
99. Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., et al. (2000). Genetic diversity and disease control in rice. Nature 406, 718-722. doi: 10.1038/35021046