1887

Abstract

Lateral gene transfer (LGT) is an important mechanism by which micro-organisms acquire new functions. This process has been suggested to be central to prokaryotic evolution in various environments. However, the influence of geographical constraints on the evolution of laterally acquired genes in microbial metabolic evolution is not yet well understood. In this study, the influence of geographical isolation on the evolution of laterally acquired dissimilatory sulphite reductase () gene sequences in the sulphate-reducing micro-organisms (SRM) was investigated. Sequences on four continental blocks related to SRM known to have received by LGT were analysed using standard phylogenetic and multidimensional statistical methods. Sequences related to lineages with large genetic diversity correlated positively with habitat divergence. Those affiliated to indicated strong biogeographical delineation; hydrothermal-vent sequences clustered independently from hot-spring sequences. Some of the hydrothermal-vent and hot-spring sequences suggested to have been acquired from a common ancestral source may have diverged upon isolation within distinct habitats. In contrast, analysis of some sequences indicated they could have been transferred from different ancestral sources but converged upon isolation within the same niche. These results hint that, after lateral acquisition of genes, barriers to gene flow probably play a strong role in their subsequent evolution.

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2011-07-01
2019-10-14
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References

  1. Bahr M. , Crump B. C. , Klepac-Ceraj V. , Teske A. , Sogin M. L. , Hobbie J. E. . ( 2005; ). Molecular characterization of sulfate-reducing bacteria in a New England salt marsh. . Environ Microbiol 7:, 1175–1185. [CrossRef].[PubMed].
    [Google Scholar]
  2. Baker B. J. , Moser D. P. , MacGregor B. J. , Fishbain S. , Wagner M. , Fry N. K. , Jackson B. , Speolstra N. , Loos S. et al. ( 2003; ). Related assemblages of sulphate-reducing bacteria associated with ultradeep gold mines of South Africa and deep basalt aquifers of Washington State. . Environ Microbiol 5:, 267–277. [CrossRef].[PubMed].
    [Google Scholar]
  3. Bamborough L. , Cummings S. J. . ( 2009; ). The impact of increasing heavy metal stress on the diversity and structure of the bacterial and actinobacterial communities of metallophytic grassland soil. . Biol Fertil Soils 45:, 273–280. [CrossRef]
    [Google Scholar]
  4. Baptista J. C. , Davenport R. J. , Donnelly T. , Curtis T. P. . ( 2008; ). The microbial diversity of laboratory-scale wetlands appears to be randomly assembled. . Water Res 42:, 3182–3190. [CrossRef].[PubMed].
    [Google Scholar]
  5. Bloom S. A. . ( 1981; ). Similarity indices in community studies: potential pitfalls. . Mar Ecol Prog Ser 5:, 125–128. [CrossRef]
    [Google Scholar]
  6. Boucher Y. , Douady C. J. , Papke R. T. , Walsh D. A. , Boudreau M. E. , Nesbø C. L. , Case R. J. , Doolittle W. F. . ( 2003; ). Lateral gene transfer and the origins of prokaryotic groups. . Annu Rev Genet 37:, 283–328. [CrossRef].[PubMed].
    [Google Scholar]
  7. Bowen J. L. , Crump B. C. , Deegan L. A. , Hobbie J. E. . ( 2009; ). Salt marsh sediment bacteria: their distribution and response to external nutrient inputs. . ISME J 3:, 924–934. [CrossRef].[PubMed].
    [Google Scholar]
  8. Castro H. , Reddy K. R. , Ogram A. . ( 2002; ). Composition and function of sulfate-reducing prokaryotes in eutrophic and pristine areas of the Florida Everglades. . Appl Environ Microbiol 68:, 6129–6137. [CrossRef].[PubMed].
    [Google Scholar]
  9. Chang Y.-J. , Peacock A. D. , Long P. E. , Stephen J. R. , McKinley J. P. , Macnaughton S. J. , Hussain A. K. M. A. , Saxton A. M. , White D. C. . ( 2001; ). Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. . Appl Environ Microbiol 67:, 3149–3160. [CrossRef].[PubMed].
    [Google Scholar]
  10. Cheng C.-C. . ( 2004; ). Statistical approaches on discriminating spatial variation of species diversity. . Bot Bull Acad Sin 45:, 339–346.
    [Google Scholar]
  11. Chi Fru E. . ( 2009; ). Iron oxides influence bacterial community structure and the spatial distribution of the aerobic methanotrophs and sulphate reducers in granitic aquifers. . Geomicrobiol J 26:, 415–429. [CrossRef]
    [Google Scholar]
  12. Chi Fru E. , Athar R. . ( 2008; ). In situ bacterial colonization of compacted bentonite under deep geological high-level radioactive waste repository conditions. . Appl Microbiol Biotechnol 79:, 499–510. [CrossRef].[PubMed].
    [Google Scholar]
  13. Clarke K. R. , Gorley R. N. . ( 2006; ). PRIMER v6: User Manual/Tutorial. Plymouth, UK:: PRIMER-E;.
    [Google Scholar]
  14. Crawford J. W. , Harris J. A. , Ritz K. , Young I. M. . ( 2005; ). Towards an evolutionary ecology of life in soil. . Trends Ecol Evol 20:, 81–87. [CrossRef].[PubMed].
    [Google Scholar]
  15. Davies K. F. , Chesson P. , Harrison S. , Inouye B. D. , Melbourne B. A. , Rice K. J. . ( 2005; ). Spatial heterogeneity explains the scale dependence of the native–exotic diversity relationship. . Ecology 86:, 1602–1610. [CrossRef]
    [Google Scholar]
  16. De Wit R. , Bouvier T. . ( 2006; ). Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say?. Environ Microbiol 8:, 755–758. [CrossRef].[PubMed].
    [Google Scholar]
  17. Dhillon A. , Teske A. , Dillon J. , Stahl D. A. , Sogin M. L. . ( 2003; ). Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. . Appl Environ Microbiol 69:, 2765–2772. [CrossRef].[PubMed].
    [Google Scholar]
  18. Gray N. D. , Brown A. , Nelson D. R. , Pickup R. W. , Rowan A. K. , Head I. M. . ( 2007; ). The biogeographical distribution of closely related freshwater sediment bacteria is determined by environmental selection. . ISME J 1:, 596–605. [CrossRef].[PubMed].
    [Google Scholar]
  19. Hammer Ø. , Harper D. A. T. , Ryan P. D. . ( 2001; ). past: paleontological statistics software package for education and data analysis. . Palaeontol Electron 4:, 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
    [Google Scholar]
  20. Huynen M. , Snel B. , Bork P. . ( 1999; ). Lateral gene transfer, genome surveys, and the phylogeny of prokaryotes. . Science 286:, 1443. [CrossRef]
    [Google Scholar]
  21. Jeanthon C. , L’Haridon S. , Cueff V. , Banta A. , Reysenbach A. L. , Prieur D. . ( 2002; ). Thermodesulfobacterium hydrogeniphilum sp. nov., a thermophilic, chemolithoautotrophic, sulfate-reducing bacterium isolated from a deep-sea hydrothermal vent at Guaymas Basin, and emendation of the genus Thermodesulfobacterium . . Int J Syst Evol Microbiol 52:, 765–772. [CrossRef].[PubMed].
    [Google Scholar]
  22. Jørgensen B. B. . ( 1982; ). Mineralization of organic matter in the sea bed – the role of sulphate reduction. . Nature 296:, 643–645. [CrossRef]
    [Google Scholar]
  23. Klein M. , Friedrich M. , Roger A. J. , Hugenholtz P. , Fishbain S. , Abicht H. , Blackall L. L. , Stahl D. A. , Wagner M. . ( 2001; ). Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. . J Bacteriol 183:, 6028–6035. [CrossRef].[PubMed].
    [Google Scholar]
  24. Lan R. T. , Reeves P. R. . ( 1996; ). Gene transfer is a major factor in bacterial evolution. . Mol Biol Evol 13:, 47–55.[PubMed].[CrossRef]
    [Google Scholar]
  25. Lee C. , Kim J. , Do H. , Hwang S. . ( 2008; ). Monitoring thiocyanate-degrading microbial community in relation to changes in process performance in mixed culture systems near washout. . Water Res 42:, 1254–1262. [CrossRef].[PubMed].
    [Google Scholar]
  26. Leloup J. , Quillet L. , Berthe T. , Petit F. . ( 2006; ). Diversity of the dsrAB (dissimilatory sulfite reductase) gene sequences retrieved from two contrasting mudflats of the Seine estuary, France. . FEMS Microbiol Ecol 55:, 230–238.[PubMed].[CrossRef]
    [Google Scholar]
  27. Liu X. , Bagwell C. E. , Wu L. , Devol A. H. , Zhou J. . ( 2003; ). Molecular diversity of sulfate-reducing bacteria from two different continental margin habitats. . Appl Environ Microbiol 69:, 6073–6081. [CrossRef].[PubMed].
    [Google Scholar]
  28. Loy A. , Küsel K. , Lehner A. , Drake H. L. , Wagner M. . ( 2004; ). Microarray and functional gene analyses of sulfate-reducing prokaryotes in low-sulfate, acidic fens reveal cooccurrence of recognized genera and novel lineages. . Appl Environ Microbiol 70:, 6998–7009. [CrossRef].[PubMed].
    [Google Scholar]
  29. Ludwig W. , Strunk O. , Westram R. , Richter L. , Meier H. , Yadhukumar , Buchner A. , Lai T. , Steppi S. et al. ( 2004; ). arb: a software environment for sequence data. . Nucleic Acids Res 32:, 1363–1371. [CrossRef].[PubMed].
    [Google Scholar]
  30. Martinez R. J. , Wang Y. , Raimondo M. A. , Coombs J. M. , Barkay T. , Sobecky P. A. . ( 2006; ). Horizontal gene transfer of PIB-type ATPases among bacteria isolated from radionuclide- and metal-contaminated subsurface soils. . Appl Environ Microbiol 72:, 3111–3118. [CrossRef].[PubMed].
    [Google Scholar]
  31. Martiny J. B. H. , Bohannan B. J. , Brown J. H. , Colwell R. K. , Fuhrman J. A. , Green J. L. , Horner-Devine M. C. , Kane M. , Krumins J. A. et al. ( 2006; ). Microbial biogeography: putting microorganisms on the map. . Nat Rev Microbiol 4:, 102–112. [CrossRef].[PubMed].
    [Google Scholar]
  32. Miletto M. , Loy A. , Antheunisse A. M. , Loeb R. , Bodelier P. L. E. , Laanbroek H. J. . ( 2008; ). Biogeography of sulfate-reducing prokaryotes in river floodplains. . FEMS Microbiol Ecol 64:, 395–406.[PubMed].[CrossRef]
    [Google Scholar]
  33. Nakagawa T. , Fukui M. . ( 2003; ). Molecular characterization of community structures and sulfur metabolism within microbial streamers in Japanese hot springs. . Appl Environ Microbiol 69:, 7044–7057. [CrossRef].[PubMed].
    [Google Scholar]
  34. Nakagawa T. , Nakagawa S. , Inagaki F. , Takai K. , Horikoshi K. . ( 2004; ). Phylogenetic diversity of sulfate-reducing prokaryotes in active deep-sea hydrothermal vent chimney structures. . FEMS Microbiol Lett 232:, 145–152. [CrossRef].[PubMed].
    [Google Scholar]
  35. Nercessian O. , Bienvenu N. , Moreira D. , Prieur D. , Jeanthon C. . ( 2005; ). Diversity of functional genes of methanogens, methanotrophs and sulfate reducers in deep-sea hydrothermal environments. . Environ Microbiol 7:, 118–132. [CrossRef].[PubMed].
    [Google Scholar]
  36. Ochman H. , Lawrence J. G. , Groisman E. A. . ( 2000; ). Lateral gene transfer and the nature of bacterial innovation. . Nature 405:, 299–304. [CrossRef].[PubMed].
    [Google Scholar]
  37. Palacios C. , Zettler E. , Amils R. , Amaral-Zettler L. . ( 2008; ). Contrasting microbial community assembly hypotheses: a reconciling tale from the Río Tinto. . PLoS ONE 3:, e3853. [CrossRef].[PubMed].
    [Google Scholar]
  38. Pérez-Jiménez J. R. , Young L. Y. , Kerkhof L. J. . ( 2001; ). Molecular characterization of sulfate-reducing bacteria in anaerobic hydrocarbon-degrading consortia and pure cultures using the dissimilatory sulfite reductase (dsrAB) genes. . FEMS Microbiol Ecol 35:, 145–150.[PubMed].[CrossRef]
    [Google Scholar]
  39. Rabus R. , Hansen T. A. , Widdel F. . ( 2006; ). Dissimilatory sulfate- and sulfur-reducing prokaryotes. . In The Prokaryotes, , 3rd edn., vol. 2, pp. 659–768. Edited by Dworkin M. , Falkow S. , Rosenberg E. , Schleifer K. H. , Stackebrandt E. . . New York:: Springer;. [CrossRef].
    [Google Scholar]
  40. Ramette A. , Tiedje J. M. . ( 2007; a). Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. . Microb Ecol 53:, 197–207. [CrossRef].[PubMed].
    [Google Scholar]
  41. Ramette A. , Tiedje J. M. . ( 2007; b). Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. . Proc Natl Acad Sci U S A 104:, 2761–2766. [CrossRef].[PubMed].
    [Google Scholar]
  42. Raup D. M. , Crick R. E. . ( 1979; ). Measurements of faunal similarity in paleontology. . J Paleontol 53:, 1213–1227.
    [Google Scholar]
  43. Reno M. L. , Held N. L. , Fields C. J. , Burke P. V. , Whitaker R. J. . ( 2009; ). Biogeography of the Sulfolobus islandicus pan-genome. . Proc Natl Acad Sci U S A 106:, 8605–8610.[CrossRef]
    [Google Scholar]
  44. Rowan A. K. , Snape J. R. , Fearnside D. , Barer M. R. , Curtis T. P. , Head I. M. . ( 2003; ). Composition and diversity of ammonia-oxidising bacterial communities in wastewater treatment reactors of different design treating identical wastewater. . FEMS Microbiol Ecol 43:, 195–206.[PubMed].[CrossRef]
    [Google Scholar]
  45. Simberloff D. . ( 1978; ). Using island biogeographic distributions to determine if colonization is stochastic. . Am Nat 112:, 713–726. [CrossRef]
    [Google Scholar]
  46. Stahl D. A. , Fishbain S. , Klein M. , Baker B. J. , Wagner M. . ( 2002; ). Origins and diversification of sulfate-respiring microorganisms. . Antonie van Leeuwenhoek 81:, 189–195. [CrossRef].[PubMed].
    [Google Scholar]
  47. Suzuki Y. , Kelly S. D. , Kemner K. M. , Banfield J. F. . ( 2005; ). Direct microbial reduction and subsequent preservation of uranium in natural near-surface sediment. . Appl Environ Microbiol 71:, 1790–1797. [CrossRef].[PubMed].
    [Google Scholar]
  48. Travouillon K. J. , Archer M. , Legendre S. , Hand S. J. . ( 2007; ). Finding the minimum sample richness (MSR) for multivariate analyses: implications for palaeoecology. . Hist Biol 19:, 315–320. [CrossRef]
    [Google Scholar]
  49. Treves D. S. , Xia B. , Zhou J. , Tiedje J. M. . ( 2003; ). A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. . Microb Ecol 45:, 20–28. [CrossRef].[PubMed].
    [Google Scholar]
  50. Trüper H. G. . ( 2003; ). Valid publication of the genus name Thermodesulfobacterium and the species names Thermodesulfobacterium commune (Zeikus et al. 1983) and Thermodesulfobacterium thermophilum (ex Desulfovibrio thermophilus Rozanova and Khudyakova 1974). Opinion 71. . Int J Syst Evol Microbiol 53:, 927. [CrossRef].[PubMed].
    [Google Scholar]
  51. Van der Gast C. J. . ( 2008; ). Island shaping thought in microbial ecology. . In Advances in Applied Microbiology, pp. 176–182. Edited by Laskin A. I. , Gadd G. M. , Sariaslani S. . . London:: Elsevier Academic Press;.
    [Google Scholar]
  52. Van der Gast C. J. , Jefferson B. , Reid E. , Robinson T. , Bailey M. J. , Judd S. J. , Thompson I. P. . ( 2006; ). Bacterial diversity is determined by volume in membrane bioreactors. . Environ Microbiol 8:, 1048–1055. [CrossRef].[PubMed].
    [Google Scholar]
  53. Van der Gast C. J. , Ager D. , Lilley A. K. . ( 2008; ). Temporal scaling of bacterial taxa is influenced by both stochastic and deterministic ecological factors. . Environ Microbiol 10:, 1411–1418. [CrossRef].[PubMed].
    [Google Scholar]
  54. Wagner M. , Roger A. J. , Flax J. L. , Brusseau G. A. , Stahl D. A. . ( 1998; ). Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. . J Bacteriol 180:, 2975–2982.[PubMed].
    [Google Scholar]
  55. Whitaker R. J. , Grogan D. W. , Taylor J. W. . ( 2003; ). Geographic barriers isolate endemic populations of hyperthermophilic archaea. . Science 301:, 976–978. [CrossRef].[PubMed].
    [Google Scholar]
  56. Zeikus J. G. , Dawson M. A. , Thompson T. E. , Ingvorsen K. , Hatchikian E. C. . ( 1983; ). Microbial ecology of volcanic sulphidogenesis: isolation and characterization of Thermodesulfotobacterium commune gen. nov. and sp. nov.. J Gen Microbiol 129:, 1159–1169.
    [Google Scholar]
  57. Zverlov V. , Klein M. , Lücker S. , Friedrich M. W. , Kellermann J. , Stahl D. A. , Loy A. , Wagner M. . ( 2005; ). Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. . J Bacteriol 187:, 2203–2208. [CrossRef].[PubMed].
    [Google Scholar]
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