Relating phylogenetic and functional diversity among denitrifiers and quantifying their capacity to predict community functioning

Frontiers in Microbiology

Volumn 3, Issue JUN, 2012, Pages

  Salles, Joana Falcão ^a   Le Roux, Xavier ^a   Poly, Franck ^a  

^a UNIVERSITÉ DE LYON   (France)

Author keywords

Biodiversity proxies; Carbon sources; Denitrification; Functional traits; Phylogenetic diversity

Indexed keywords

EID: 84875769694     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00209     Document Type: Article

References (62)

1. Allison, S. D., and Martiny, J. B. H. (2008). Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. U.S.A. 105, 11512-11519.
2. Attard, E., Poly, F., Commeaux, C., Laurent, F., Terada, A., Smets, B. F., Recous, S., and Le Roux, X. (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.
3. Attard, E., Recous, S., Chabbi, A., De Berranger, C., Guillaumaud, N., Labreuche, J., Philippot, L., Schmid, B., and Le Roux, X. (2011). Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land-uses. Glob. Chang. Biol. 17, 1975-1989.
4. Baelum, J., Jacobsen, C. S., and Holben, W. E. (2010). Comparison of 16S rRNA gene phylogeny and functional tfdA gene distribution in thirty-one different 2,4-dichlorophenoxyacetic acid and 4-chloro-2-methylphenoxyacetic acid degraders. Syst. Appl. Microbiol. 33, 67-70.
5. Bärlocher, F., and Corkum, M. (2003). Nutrient enrichment overwhelms diversity effects in leaf decomposition by stream fungi. Oikos 101, 247-252.
6. 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.
7. Bruce, K. D., Hiorns, W. D., Hobman, J. L., Osborn, A. M., Strike, P., and Ritchie, D. A. (1992). Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl. Environ. Microbiol. 58, 3413-3416.
8. Cadotte, M. W., Cavender-Bares, J., Tilman, D., and Oakley, T. H. (2009). Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4, e5695. doi:10.1371/journal.pone.0005695
9. Carlson, C. A., and Ingraham, J. L. (1983). Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans. Appl. Environ. Microbiol. 45, 1247-1253.
10. Cavigelli, M. A., and Robertson, G. P. (2000). The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81, 1402-1414.
11. Cohan, F. M. (2006). Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1985-1996.
12. Cole, J. R., Chai, B., Farris, R. J., Wang, Q., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Bandela, A. M., Cardenas, E., Garrity, G. M., and Tiedje, J. M. (2007). The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 35, D169-D172.
13. Fierer, N., Bradford, M. A., and Jackson, R. B. (2007). Toward and ecological classification of soil bacteria. Ecology 88, 1354-1364.
14. Fierer, N., Lauber, C., Ramirez, K. S., Zaneveld, J., Bradford, M. A., and Knight, R. (2012). Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 6, 1007-1017.
15. Gans, J., Wolinsky, M., and Dunbar, J. (2005). Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309, 1387-1390.
16. Giller, P. S., Hillebrand, H., Berninger, U.-G., Gessner, M. O., Hawkins, S., Inchausti, P., Inglis, C., Leslie, H., Malmqvist, B., Monaghan, M. T., Morin, P. J., and O'Mullan, G. (2004). Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104, 423-436.
17. Goldfarb, K. C., Karaoz, U., Hanson, C. A., Santee, C. A., Bradford, M. A., Treseder, K. K., Wallenstein, M. D., and Brodiie, E. L. (2011). Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front. Microbiol. 2:94. doi:10.3389/fmicb.2011.00094
18. Gonnet, G. H., Cohen, M. A., and Benner, S. A. (1992). Exhaustive matching of the entire protein sequence database. Science 256, 1443-1445.
19. Hallin, S., Jones, C. M., Schloter, M., and Philippot, L. (2009). Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J. 3, 597-605.
20. Heemsbergen, D. A., Berg, M. P., Verhoef, H. A., van Hal, J. R., Faber, J. H., and Loreau, M. (2004). Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306, 1019-1020.
21. Heylen, K., Gevers, D., Vanparys, B., Wittebolle, L., Geets, J., Boon, N., and De Vos, P. (2006). The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ. Microbiol. 8, 2012-2021.
22. Hooper,D. U.,Chapin,F. S. III,Ewel,J. J., Hector, A., Schmid, B., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Setäla, H., Symstad, A. J., Vandermeer, J., and Wardle, D. A. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3-35.
23. Hooper, D. U., Solan, M., Symstad, A. J., Diaz, S., Gessner, M. O., Buchmann, N., Degrange, V., Grime, P., Hulot, F., Mermillod-Blondin, F., Roy, J., Sphen, E., and van Peer, L. (2002). "Species diversity, functional diversity, and ecosystem functioning," in Biodiversity and Ecosystem Functioning: Synthesis and Perspectives,eds M. Loreau, S. Naeem, and P. Inchausti (Oxford: Oxford University Press), 195-208.
24. Jiang, L. (2007). Negative selection effects suppress relationships between bacterial diversity and ecosystem fucntioning. Ecology 88, 1075-1085.
25. Jones, C. M., and Hallin, S. (2010). Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J. 4, 633-641.
26. Jones, C. M., Stres, B., Rosenquist, M., and Hallin, S. (2008). Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol. Biol. Evol. 25, 1955-1966.
27. Jousset, A., Schmid, B., Scheu, S., and Eisenhauer, N. (2011). Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol. Lett. 14, 537-545.
28. Jukes, T. H., and Cantor, C. R. (1969). "Evolution of protein molecules," in Mammalian Protein Metabolism,ed. H. N. Munro (New York, NY: Academic Press), 21-132.
29. Kandeler, E., Deiglmayr, K., Tscherko, D., Bru, D., and Philippot, L. (2006). Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a Glacier Foreland. Appl. Environ. Microbiol. 72, 5957-5962.
30. 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.
31. Le Roux, X., Poly, F., Currey, P., Commeaux, C., Hai, B., Nicol, G. W., Prosser, J. I., Schloter, M., Attard, E., and Klumpp, K. (2008). Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure. ISME J. 2, 221-232.
32. Leps, J., and Smilauer, P. (2003). Mutivariate Analysis of Ecologicla Data Using CANOCO. Cambridge: Cambridge University Press.
33. Liu, X. D., Tiquia, S. M., Holguin, G., Wu, L. Y., Nold, S. C., Devol, A. H., Luo, K., Palumbo, A. V., Tiedje, J. M., and Zhou, J. Z. (2003). Molecular diversity of denitrifying genes in continental margin sediments within the oxygen-deficient zone off the Pacific coast of Mexico. Appl. Environ. Microbiol. 69, 3549-3560.
34. Losos, J. B. (2008). Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett. 11, 995-1007.
35. Mahne, I., and Tiedje, J. M. (1995). Criteria and methodology for identifying respiratory denitrifiers. Appl. Environ. Microbiol. 61, 1110-1115.
36. Mouchet, M. A., Villéger, S., Mason, N. W. H., and Mouillot, D. (2010). Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct. Ecol. 24, 867-876.
37. Mouillot, D. (2007). Niche-assembly vs. dispersal-assembly rules in coastal fish metacommunities: implications for management of biodiversity in brackish lagoons. J. Appl. Ecol. 44, 760-767.
38. Naeem, S., and Wright, J. P. (2003). Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol. Lett. 6, 567-579.
39. Patra, A. K., Abbadie, L., Clays-Josserand, A., Degrange, V., Grayston, S. J., Loiseau, P., Louault, F., Mahmood, S., Nazaret, S., Philippot, L., Poly, F., Prosser, J. I., Richaume, A., and Le Roux, X. (2005). Effects of grazing on microbial functional groups involved in soils dynamics. Ecol. Monogr. 75, 65-80.
40. Petchey, O. L. (2004). On the statistical significance of functional diversity effects. Funct. Ecol. 18, 297-303.
41. Petchey, O. L., and Gaston, K. J. (2002). Functional diversity (FD), species richness and community composition. Ecol. Lett. 5, 402-411.
42. Petchey, O. L., and Gaston, K. J. (2006). Functional diversity: back to basics and looking forward. Ecol. Lett. 9, 741-758.
43. Petchey, O. L., O'Gorman, E. J., and Flynn, D. F. B. (2009). "A functional guide to functional diversity measures," in Biodiversity, Ecosystem Functioning, and Human Wellbeing: An Ecological and Economic Perspective, eds S. Naeem, D. E. Bunker, A. Hector, M. Loreau, and C. Perrings (Great Britain: Oxford University Press), 49-59.
44. Philippot, L., Andersson, S. G. E., Battin, T. J., Prosser, J. I., Schimel, J. P., Whitman, W. B., and Hallin, S. (2010). The ecological coherence of high bacterial taxonomic ranks. Nat. Rev. Microbiol. 8, 523-529.
45. Philippot, L., and Hallin, S. (2005). Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr. Opin. Microbiol. 8, 234-239.
46. Philippot, L., Hallin, S., and Schloter, M. (2007). Ecology of denitrifying prokaryotes in agricultural soil. Adv. Agron. 96, 249-305.
47. Poly, F., Wertz, S., Brothier, E., and Degrange, V. (2008). First exploration of Nitrobacter diversity in soils by a PCR cloning-sequencing approach targeting functional gene nxrA. FEMS Microbiol. Ecol. 63, 132-140.
48. Prosser, J. I., and Nicol, G. W. (2008). Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931-2941.
49. Sambrook, J., Fritisch, E. F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Second Edn. New York: Cold Spring Harbor Laboratory Press.
50. Salles, J. F., Poly, F., Schmid, B., and Le Roux, X. (2009). Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology 90, 3324-3332.
51. Setäla, H., and McLean, M. A. (2004). Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139, 98-107.
52. Sharma, S., Aneja, M. K., Mayer, J., Munch, J. C., and Schloter, M. (2005). Diversity of transcripts of nitrite reductase genes (nirK and nirS) in rhizospheres of grain legumes. Appl. Environ. Microbiol. 71, 2001-2007.
53. Smith, J. M., and Ogram, A. (2008). Genetic and functional variation in denitrifier populations along a short-term restoration chronosequence. Appl. Environ. Microbiol. 74, 5615-5620.
54. Stephen, J. R., McCaig, A. E., Smith, Z., Prosser, J. I., and Embley, T. M. (1996). Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 62, 4147-4154.
55. Strickland, M. S., Lauber, C., Fierer, N., and Bradford, M. A. (2009). Testing the functional significance of microbial community composition. Ecology 90, 441-451.
56. Throback, I. N., Enwall, K., Jarvis, A., and Hallin, S. (2004). Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol. Ecol. 49, 401-417.
57. Tiunov, A. V., and Scheu, S. (2005). Facilitative interactions rather than resource partitioning drive diversity-functioning relationships in laboratory fungal communities. Ecol. Lett. 8, 618-625.
58. Torsvik, V., and Ovreas, L. (2002). Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5, 240-245.
59. Walker, B., Kinzig, A., and Langridge, J. (1999). Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2, 95-113.
60. Wertz, S., Degrange, V., Prosser, J. I., Poly, F., Commeaux, C., Freitag, T., Guillaumaud, N., and Le Roux, X. (2006). Maintenance of soil functioning following erosion of microbial diversity. Environ. Microbiol. 8, 2162-2169.
61. 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.
62. Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533-616.