1887

Abstract

Members of the order are obligate extreme halophiles that belong to the domain . The classification of the currently relies on a polyphasic approach, which integrates phenotypic, genotypic and chemotaxonomic characterization. However, the most utilized genetic marker for phylogeny, the 16S rRNA gene, has multiple drawbacks for use with the : the species of many genera exhibit large intragenic differences between multiple ribosomal RNA operons, the gene is too conserved to discriminate reliably at the species level and it appears to be the most frequently recombined gene between closely related species. Moreover, the is a rapidly expanding group due to recent successes at cultivating novel strains from a diverse set of hypersaline environments; a fast, reliable, inexpensive, portable molecular method for discriminating species is required for their investigation. Recently, multilocus sequence analysis (MLSA) has been shown to be an effective tool for strain identification and taxonomic designation, even for those taxa that experience frequent lateral gene transfer and homologous recombination. In this study, MLSA was utilized for evolutionary and taxonomic investigation of the . Efficacy of the MLSA approach was tested across a hierarchical gradient using 52 halobacterial strains, representing 33 species (including names without standing in nomenclature) and 14 genera. A subset of 21 strains from the genus was analysed separately to test the sensitivity and relevance of the MLSA approach among closely related strains and species. The results demonstrated that MLSA differentiated individual strains, reliably grouped strains into species and species into genera and identified potential novel species and also family-like relationships. This study demonstrates that MLSA is a rapid and informative molecular method that will probably accommodate strain analysis at any taxonomic level within the .

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.029298-0
2011-12-01
2019-12-11
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/61/12/2984.html?itemId=/content/journal/ijsem/10.1099/ijs.0.029298-0&mimeType=html&fmt=ahah

References

  1. Abascal F. , Zardoya R. , Posada D. . ( 2005; ). ProtTest: selection of best-fit models of protein evolution. . Bioinformatics 21:, 2104–2105. [CrossRef] [PubMed]
    [Google Scholar]
  2. Andam C. P. , Williams D. , Gogarten J. P. . ( 2010; ). Natural taxonomy in light of horizontal gene transfer. . Biol Philos 25:, 589–602. [CrossRef]
    [Google Scholar]
  3. Asker D. , Ohta Y. . ( 2002; ). Haloferax alexandrinus sp. nov., an extremely halophilic canthaxanthin-producing archaeon from a solar saltern in Alexandria (Egypt). . Int J Syst Evol Microbiol 52:, 729–738. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bodaker I. , Sharon I. , Suzuki M. T. , Feingersch R. , Shmoish M. , Andreishcheva E. , Sogin M. L. , Rosenberg M. , Maguire M. E. et al. & other authors ( 2010; ). Comparative community genomics in the Dead Sea: an increasingly extreme environment. . ISME J 4:, 399–407. [CrossRef] [PubMed]
    [Google Scholar]
  5. Boucher Y. , Douady C. J. , Sharma A. K. , Kamekura M. , Doolittle W. F. . ( 2004; ). Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. . J Bacteriol 186:, 3980–3990. [CrossRef] [PubMed]
    [Google Scholar]
  6. Casamayor E. O. , Massana R. , Benlloch S. , Øvreås L. , Díez B. , Goddard V. J. , Gasol J. M. , Joint I. , Rodríguez-Valera F. , Pedrós-Alió C. . ( 2002; ). Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. . Environ Microbiol 4:, 338–348. [CrossRef] [PubMed]
    [Google Scholar]
  7. Case R. J. , Boucher Y. , Dahllöf I. , Holmström C. , Doolittle W. F. , Kjelleberg S. . ( 2007; ). Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. . Appl Environ Microbiol 73:, 278–288. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cuadros-Orellana S. , Martin-Cuadrado A. B. , Legault B. , D’Auria G. , Zhaxybayeva O. , Papke R. T. , Rodriguez-Valera F. . ( 2007; ). Genomic plasticity in prokaryotes: the case of the square haloarchaeon. . ISME J 1:, 235–245. [CrossRef] [PubMed]
    [Google Scholar]
  9. Edgar R. C. . ( 2004a; ). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. . BMC Bioinformatics 5:, 113. [CrossRef] [PubMed]
    [Google Scholar]
  10. Edgar R. C. . ( 2004b; ). MUSCLE: multiple sequence alignment with high accuracy and high throughput. . Nucleic Acids Res 32:, 1792–1797. [CrossRef] [PubMed]
    [Google Scholar]
  11. Enache M. , Itoh T. , Fukushima T. , Usami R. , Dumitru L. , Kamekura M. . ( 2007; ). Phylogenetic relationships within the family Halobacteriaceae inferred from rpoB′ gene and protein sequences. . Int J Syst Evol Microbiol 57:, 2289–2295. [CrossRef] [PubMed]
    [Google Scholar]
  12. Guindon S. , Gascuel O. . ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52:, 696–704. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hanage W. P. , Fraser C. , Spratt B. G. . ( 2005; ). Fuzzy species among recombinogenic bacteria. . BMC Biol 3:, 6. [CrossRef] [PubMed]
    [Google Scholar]
  14. Kamaishi T. , Hashimoto T. , Nakamura Y. , Nakamura F. , Murata S. , Okada N. , Okamoto K. , Shimizu M. , Hasegawa M. . ( 1996; ). Protein phylogeny of translation elongation factor EF-1 alpha suggests microsporidians are extremely ancient eukaryotes. . J Mol Evol 42:, 257–263. [CrossRef] [PubMed]
    [Google Scholar]
  15. Le S. Q. , Gascuel O. . ( 2008; ). An improved general amino acid replacement matrix. . Mol Biol Evol 25:, 1307–1320. [CrossRef] [PubMed]
    [Google Scholar]
  16. Legault B. A. , Lopez-Lopez A. , Alba-Casado J. C. , Doolittle W. F. , Bolhuis H. , Rodriguez-Valera F. , Papke R. T. . ( 2006; ). Environmental genomics of “Haloquadratum walsbyi” in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. . BMC Genomics 7:, 171. [CrossRef] [PubMed]
    [Google Scholar]
  17. López-López A. , Benlloch S. , Bonfá M. , Rodríguez-Valera F. , Mira A. . ( 2007; ). Intragenomic 16S rDNA divergence in Haloarcula marismortui is an adaptation to different temperatures. . J Mol Evol 65:, 687–696. [CrossRef] [PubMed]
    [Google Scholar]
  18. Maddison W. P. , Maddison D. R. . ( 2009; ). Mesquite: a modular system for evolutionary analysis, version 2.71. . http://mesquiteproject.org.
  19. Maiden M. C. , Bygraves J. A. , Feil E. , Morelli G. , Russell J. E. , Urwin R. , Zhang Q. , Zhou J. , Zurth K. et al. & other authors ( 1998; ). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. . Proc Natl Acad Sci U S A 95:, 3140–3145. [CrossRef] [PubMed]
    [Google Scholar]
  20. Minegishi H. , Kamekura M. , Itoh T. , Echigo A. , Usami R. , Hashimoto T. . ( 2010; ). Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B′ (rpoB′) gene. . Int J Syst Evol Microbiol 60:, 2398–2408. [CrossRef] [PubMed]
    [Google Scholar]
  21. Nakamura L. K. , Roberts M. S. , Cohan F. M. . ( 1999; ). Relationship of Bacillus subtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillus subtilis subsp. spizizenii subsp. nov. . Int J Syst Bacteriol 49:, 1211–1215. [CrossRef] [PubMed]
    [Google Scholar]
  22. Ochsenreiter T. , Pfeifer F. , Schleper C. . ( 2002; ). Diversity of Archaea in hypersaline environments characterized by molecular-phylogenetic and cultivation studies. . Extremophiles 6:, 267–274. [CrossRef] [PubMed]
    [Google Scholar]
  23. Oren A. . ( 1994; ). The ecology of the extremely halophilic archaea. . FEMS Microbiol Rev 13:, 415–439. [CrossRef]
    [Google Scholar]
  24. Oren A. . ( 2008; ). Microbial life at high salt concentrations: phylogenetic and metabolic diversity. . Saline Syst 4:, 2.[PubMed] [CrossRef]
    [Google Scholar]
  25. Oren A. , Ventosa A. . ( 2000; ). International Committee on Systematic Bacteriology Subcommittee on the taxonomy of Halobacteriaceae. Minutes of the meetings, 16 August 1999, Sydney, Australia. . Int J Syst Evol Microbiol 50:, 1405–1407. [CrossRef] [PubMed]
    [Google Scholar]
  26. Oren A. , Ginzburg M. , Ginzburg B. Z. , Hochstein L. I. , Volcani B. E. . ( 1990; ). Haloarcula marismortui (Volcani) sp. nov., nom. rev., an extremely halophilic bacterium from the Dead Sea. . Int J Syst Bacteriol 40:, 209–210. [CrossRef] [PubMed]
    [Google Scholar]
  27. Oren A. , Ventosa A. , Gutiérrez M. C. , Kamekura M. . ( 1999; ). Haloarcula quadrata sp. nov., a square, motile archaeon isolated from a brine pool in Sinai (Egypt). . Int J Syst Bacteriol 49:, 1149–1155. [CrossRef] [PubMed]
    [Google Scholar]
  28. Papke R. T. . ( 2009; ). A critique of prokaryotic species concepts. . Methods Mol Biol 532:, 379–395. [CrossRef] [PubMed]
    [Google Scholar]
  29. Papke R. T. , Douady C. J. , Doolittle W. F. , Rodríguez-Valera F. . ( 2003; ). Diversity of bacteriorhodopsins in different hypersaline waters from a single Spanish saltern. . Environ Microbiol 5:, 1039–1045. [CrossRef] [PubMed]
    [Google Scholar]
  30. Papke R. T. , Koenig J. E. , Rodríguez-Valera F. , Doolittle W. F. . ( 2004; ). Frequent recombination in a saltern population of Halorubrum. . Science 306:, 1928–1929.[PubMed]
    [Google Scholar]
  31. Papke R. T. , Zhaxybayeva O. , Feil E. J. , Sommerfeld K. , Muise D. , Doolittle W. F. . ( 2007; ). Searching for species in haloarchaea. . Proc Natl Acad Sci U S A 104:, 14092–14097. [CrossRef] [PubMed]
    [Google Scholar]
  32. Pasić L. , Ulrih N. P. , Crnigoj M. , Grabnar M. , Velikonja B. H. . ( 2007; ). Haloarchaeal communities in the crystallizers of two adriatic solar salterns. . Can J Microbiol 53:, 8–18. [CrossRef] [PubMed]
    [Google Scholar]
  33. Posada D. . ( 2008; ). jModelTest: phylogenetic model averaging. . Mol Biol Evol 25:, 1253–1256. [CrossRef] [PubMed]
    [Google Scholar]
  34. Renesto P. , Gouvernet J. , Drancourt M. , Roux V. , Raoult D. . ( 2001; ). Use of rpoB gene analysis for detection and identification of Bartonella species. . J Clin Microbiol 39:, 430–437. [CrossRef] [PubMed]
    [Google Scholar]
  35. Sandler S. J. , Hugenholtz P. , Schleper C. , DeLong E. F. , Pace N. R. , Clark A. J. . ( 1999; ). Diversity of radA genes from cultured and uncultured archaea: comparative analysis of putative RadA proteins and their use as a phylogenetic marker. . J Bacteriol 181:, 907–915.[PubMed]
    [Google Scholar]
  36. Sheppard S. K. , McCarthy N. D. , Falush D. , Maiden M. C. . ( 2008; ). Convergence of Campylobacter species: implications for bacterial evolution. . Science 320:, 237–239. [CrossRef] [PubMed]
    [Google Scholar]
  37. Shimodaira H. . ( 2002; ). An approximately unbiased test of phylogenetic tree selection. . Syst Biol 51:, 492–508. [CrossRef] [PubMed]
    [Google Scholar]
  38. Shimodaira H. , Hasegawa M. . ( 2001; ). CONSEL: for assessing the confidence of phylogenetic tree selection. . Bioinformatics 17:, 1246–1247. [CrossRef] [PubMed]
    [Google Scholar]
  39. Stamatakis A. . ( 2006; ). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. . Bioinformatics 22:, 2688–2690. [CrossRef] [PubMed]
    [Google Scholar]
  40. Swofford D. L. . ( 2003; ). paup*: phylogenetic analysis using parsimony, version 4.0b10. . Sunderland, MA:: Sinauer Associates;.
  41. Tamura K. , Nei M. . ( 1993; ). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. . Mol Biol Evol 10:, 512–526.[PubMed]
    [Google Scholar]
  42. Tavaré S. . ( 1986; ). Some probabilistic and statistical problems in the analysis of DNA sequences. . In Lectures on Mathematics in the Life Sciences (Some Mathematical Questions in Biology), vol. 17, pp. 57–86. Edited by Miura R. M. . . Providence, RI:: American Mathematical Society;.
    [Google Scholar]
  43. Urwin R. , Maiden M. C. . ( 2003; ). Multi-locus sequence typing: a tool for global epidemiology. . Trends Microbiol 11:, 479–487. [CrossRef] [PubMed]
    [Google Scholar]
  44. Ventosa A. . ( 2001; ). Genus II. Haloarcula . . In Bergey’s Manual of Systematic Bacteriology, , 2nd edn., vol. 1, pp. 305–309. Edited by Boone D. R. , Castenholz R. W. , Garrity G. M. . . New York:: Springer;.
    [Google Scholar]
  45. Walsh D. A. , Bapteste E. , Kamekura M. , Doolittle W. F. . ( 2004; ). Evolution of the RNA polymerase B′ subunit gene (rpoB′) in Halobacteriales: a complementary molecular marker to the SSU rRNA gene. . Mol Biol Evol 21:, 2340–2351. [CrossRef] [PubMed]
    [Google Scholar]
  46. Whelan S. , Goldman N. . ( 2001; ). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. . Mol Biol Evol 18:, 691–699.[PubMed] [CrossRef]
    [Google Scholar]
  47. Young J. M. , Park D. C. , Shearman H. M. , Fargier E. . ( 2008; ). A multilocus sequence analysis of the genus Xanthomonas. . Syst Appl Microbiol 31:, 366–377. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.029298-0
Loading
/content/journal/ijsem/10.1099/ijs.0.029298-0
Loading

Data & Media loading...

Supplements

vol. , part 12, pp. 2984 - 2995

Media for cultivation of strains that have been assigned to species without validly published names or have not been deposited to culture collections. [PDF](78 KB)



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error