What is the extent of prokaryotic diversity?
Abstract
The extent of microbial diversity is an intrinsically fascinating subject of profound practical importance. The term ‘diversity’ may allude to the number of taxa or species richness as well as their relative abundance. There is uncertainty about both, primarily because sample sizes are too small. Non-parametric diversity estimators make gross underestimates if used with small sample sizes on unevenly distributed communities. One can make richness estimates over many scales using small samples by assuming a species/taxa-abundance distribution. However, no one knows what the underlying taxa-abundance distributions are for bacterial communities. Latterly, diversity has been estimated by fitting data from gene clone libraries and extrapolating from this to taxa-abundance curves to estimate richness. However, since sample sizes are small, we cannot be sure that such samples are representative of the community from which they were drawn. It is however possible to formulate, and calibrate, models that predict the diversity of local communities and of samples drawn from that local community. The calibration of such models suggests that migration rates are small and decrease as the community gets larger. The preliminary predictions of the model are qualitatively consistent with the patterns seen in clone libraries in ‘real life’. The validation of this model is also confounded by small sample sizes. However, if such models were properly validated, they could form invaluable tools for the prediction of microbial diversity and a basis for the systematic exploration of microbial diversity on the planet.
References
Bell G . 2000The distribution of abundance in neutral communities. Am. Nat. 155, 606–617.doi:10.1086/303345. . Crossref, PubMed, ISI, Google ScholarBell G . 2001Ecology—neutral macroecology. Science. 293, 2413–2418.doi:10.1126/science.293.5539.2413. . Crossref, PubMed, ISI, Google ScholarBorneman J& Triplett E.W . 1997Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl. Environ. Microbiol. 63, 2647–2653. Crossref, PubMed, ISI, Google ScholarChao A . 1984Nonparametric-estimation of the number of classes in a population. Scand. J. Stat. 11, 265–270. ISI, Google ScholarChao A . 1987Estimating the population-size for capture recapture data with unequal catchability. Biometrics. 43, 783–791.doi:10.2307/2531532. . Crossref, PubMed, ISI, Google ScholarColwell R.K& Coddington J.A . 1994Estimating terrestrial biodiversity through extrapolation. Phil. Trans. R. Soc. B. 345, 101–118. Link, ISI, Google ScholarCoskuner G, Ballinger S.J, Davenport R.J, Pickering R.L, Solera R, Head I.M& Curtis T.P . 2005Agreement between theory and measurement in quantification of ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 71, 6325–6334.doi:10.1128/AEM.71.10.6325-6334.2005. . Crossref, PubMed, ISI, Google Scholar- Curtis, T. P., Sloan, W. & Scannell, J. 2001 The estimation of prokaryotic diversity and its limits. In Nineth Int. Symp. on Microbial Ecology, Amsterdam. Google Scholar
Curtis T.P, Sloan W& Scannell J . 2002Estimating prokaryotic diversity and it limits. Proc. Natl Acad. Sci. USA. 99, 10 494–10 499.doi:10.1073/pnas.142680199. . Crossref, ISI, Google Scholar- Curtis, T. P., Baptista, J. C. & Sloan, W. T. In preparation. Estimating migration rates in microbial communities. Google Scholar
Drake J.W . 1991A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl Acad. Sci. USA. 88, 7160–7164.doi:10.1073/pnas.88.16.7160. . Crossref, PubMed, ISI, Google ScholarDunbar J, Barns S.M, Ticknor L.O& Kuske C.R . 2002Empirical and theoretical bacterial diversity in four Arizona soils. Appl. Environ. Microbiol. 68, 3035–3045.doi:10.1128/AEM.68.6.3035-3045.2002. . Crossref, PubMed, ISI, Google ScholarFenchel T& Finlay B.J . 2006The diversity of microbes: resurgence of the phenotype. Phil. Trans. R. Soc. B. 361, 1965–1973.doi:10.1098/rstb.2006.1924. . Link, ISI, Google ScholarFinlay B.J& Clarke K.J . 1999Ubiquitous dispersal of microbial species. Nature. 400, 828doi:10.1038/23616. . Crossref, ISI, Google ScholarFulthorpe R.R, Rhodes A.N& Tiedje J.M . 1998High levels of endemicity of 3-chlorobenzoate-degrading soil bacteria. Appl. Environ. Microbiol. 64, 1620–1627. Crossref, PubMed, ISI, Google ScholarGans J, Wolinsky M& Dunbar J . 2005Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science. 309, 1387–1390.doi:10.1126/science.1112665. . Crossref, PubMed, ISI, Google ScholarGodon J.J, Zumstein E, Dabert P, Habouzit F& Moletta R . 1997Molecular microbial diversity of an anaerobic digestor as determined by small-subunit rDNA sequence analysis. Appl. Environ. Microbiol. 63, 2802–2813. Crossref, PubMed, ISI, Google ScholarHagstrom A, Pommier T, Rohwer F, Simu K, Stolte W, Svensson D& Zweifel U.L . 2002Use of 16S ribosomal DNA for delineation of marine bacterioplankton species. Appl. Environ. Microbiol. 68, 3628–3633.doi:10.1128/AEM.68.7.3628-3633.2002. . Crossref, PubMed, ISI, Google ScholarHong S.H, Bunge J, Jeon S.O& Epstein S.S . 2006Predicting microbial species richness. Proc. Natl Acad. Sci. USA. 103, 117–122.doi:10.1073/pnas.0507245102. . Crossref, PubMed, ISI, Google ScholarHorner-Devine M.C, Leibold M.A, Smith V.H& Bohannan B.J.M . 2003Bacterial diversity patterns along a gradient of primary productivity. Ecol. Lett. 6, 613–622.doi:10.1046/j.1461-0248.2003.00472.x. . Crossref, ISI, Google ScholarHouchmandzadeh B& Vallade M . 2003Clustering in neutral ecology. Phys. Rev. E. 68, 061912doi:10.1103/PhysRevE.68.061912. . Crossref, ISI, Google ScholarHubbell S.P The unified neutral theory of biodiversity and biogeography. 2001Princeton, NJ:Princeton University Press. Google ScholarHugenholtz P, Goebel B.M& Pace N.R . 1998Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765–4774. Crossref, PubMed, ISI, Google ScholarLoisel P, Harmand J, Zemb O, Latrille E, Lobry C, Delgenes J.P& Godon J.J . 2006Denaturing gradient electrophoresis (DGE) and single-strand conformation polymorphism (SSCP) molecular fingerprintings revisited by simulation and used as a tool to measure microbial diversity. Environ. Microbiol. 8, 720–731.doi:10.1111/j.1462-2920.2005.00950.x. . Crossref, PubMed, ISI, Google ScholarLunn M, Sloan W.T& Curtis T.P . 2004Estimating bacterial diversity from clone libraries with flat rank abundance distributions. Environ. Microbiol. 6, 1081–1085.doi:10.1111/j.1462-2920.2004.00641.x. . Crossref, PubMed, ISI, Google ScholarMacArthur R . 1957On the relative abundance of bird species. Proc. Natl Acad. Sci. USA. 43, 293–295.doi:10.1073/pnas.43.3.293. . Crossref, PubMed, ISI, Google ScholarMacArthur R . 1960On the relative abundance of species. Am. Nat. 874, 25–36.doi:10.1086/282106. . Crossref, ISI, Google ScholarMacArthur R& Wilson E The theory of island biogeography. 1967Princeton, NJ:Princeton Univerity Press. Google ScholarMaurer B.A& McGill B.J . 2004Neutral and non-neutral macroecology. Basic Appl. Ecol. 5, 413–422.doi:10.1016/j.baae.2004.08.006. . Crossref, ISI, Google ScholarMay R.M Patterns of species abundance and diversity. Ecology and evolution of communities, Cody M.L& Diamond J.M . 1974pp. 81–120. Eds. Cambridge, MA:Harvard University Press. Google ScholarMcKane A.J, Alonso D& Sole R.V . 2004Analytic solution of Hubbell's model of local community dynamics. Theor. Popul. Biol. 65, 67–73.doi:10.1016/j.tpb.2003.08.001. . Crossref, PubMed, ISI, Google ScholarMuyzer G, Dewaal E.C& Uitterlinden A.G . 1993Profiling of complex microbial-populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16s ribosomal-RNA. Appl. Environ. Microbiol. 59, 695–700. Crossref, PubMed, ISI, Google ScholarNarang R& Dunbar J . 2004Modeling bacterial species abundance from small community surveys. Microb. Ecol. 47, 396–406.doi:10.1007/s00248-003-1026-7. . Crossref, PubMed, ISI, Google ScholarPounds J.A& Puschendorf R . 2004Ecology—clouded futures. Nature. 427, 107–109.doi:10.1038/427107a. . Crossref, PubMed, ISI, Google ScholarRoberts M.S& Cohan F.M . 1995Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis. Evolution. 49, 1081–1094.doi:10.2307/2410433. . Crossref, PubMed, ISI, Google ScholarSchloss P.D& Handelsman J . 2004Status of the microbial census. Microbiol. Mol. Biol. Rev. 68, 686–691.doi:10.1128/MMBR.68.4.686-691.2004. . Crossref, PubMed, ISI, Google ScholarSchloss P.D& Handelsman J . 2005Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71, 1501–1506.doi:10.1128/AEM.71.3.1501-1506.2005. . Crossref, PubMed, ISI, Google ScholarSchloss P.D& Handelsman J . 2006Toward a census of bacteria in soil. PLoS Comput. Biol. 2, 786–793. Crossref, ISI, Google ScholarSlatkin M& Maddison W.P . 1989A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics. 123, 603–613. Crossref, PubMed, ISI, Google ScholarSloan W.T, Lunn M, Woodcock S, Head I.M, Nee S& Curtis T.P . 2006Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ. Microbiol. 8, 732–740.doi:10.1111/j.1462-2920.2005.00956.x. . Crossref, PubMed, ISI, Google Scholar- Sloan, W. T., Woodcock, S., Head, I. M., Lunn, M. & Curtis, T. P. In press. Using environmental genomic data to identifying patterns in the structure of microbial communities. Microb. Ecol. Google Scholar
Thompson J.R, Pacocha S, Pharino C, Klepac-Ceraj V, Hunt D.E, Benoit J, Sarma-Rupavtarm R, Distel D.L& Polz M.F . 2005Genotypic diversity within a natural coastal bacterioplankton population. Science. 307, 1311–1313.doi:10.1126/science.1106028. . Crossref, PubMed, ISI, Google ScholarTorsvik V, Goksoyr J& Daae F.L . 1990High diversity in DNA of soil bacteria. Appl. Environ. Microbiol. 56, 782–787. Crossref, PubMed, ISI, Google ScholarVallade M& Houchmandzadeh B . 2003Analytical solution of a neutral model of biodiversity. Phys. Rev. E. 68, 061902doi:10.1103/PhysRevE.68.061902. . Crossref, ISI, Google ScholarVolkov I, Banavar J.R, Hubbell S.P& Maritan A . 2003Neutral theory and relative species abundance in ecology. Nature. 424, 1035–1037.doi:10.1038/nature01883. . Crossref, PubMed, ISI, Google ScholarWagner M& Loy A . 2002Bacterial community composition and function in sewage treatment systems. Curr. Opin. Biotechnol. 13, 218–227. Crossref, PubMed, ISI, Google ScholarWhitaker R.J, Grogan D.W& Taylor J.W . 2003Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science. 301, 976–978.doi:10.1126/science.1086909. . Crossref, PubMed, ISI, Google ScholarWhitman W.B, Coleman D.C& Wiebe W.J . 1998Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA. 95, 6578–6583.doi:10.1073/pnas.95.12.6578. . Crossref, PubMed, ISI, Google ScholarWoodcock S, Curtis T.P, Head I.M, Lunn M& Sloan W.T . 2006Taxa–area relationships for microbes: the unsampled and the unseen. Ecol. Lett. 9, 805–812. Crossref, PubMed, ISI, Google Scholar- Woodcock, S., van der Gast, C. J., Bell, T., Lunn, M., Curtis, T. P., Head, I. M. & Sloan, W. T. In preparation. Neutral assembly of bacterial communities. Google Scholar
Zwart G, 2003Rapid screening for freshwater bacterial groups by using reverse line blot hybridization. Appl. Environ. Microbiol. 69, 5875–5883.doi:10.1128/AEM.69.10.5875-5883.2003. . Crossref, PubMed, ISI, Google Scholar