1887

Abstract

Multilocus sequence analysis (MLSA) protocols have been developed for species circumscription for many taxa. However, at present, no studies based on MLSA have been performed within any moderately halophilic bacterial group. To test the usefulness of MLSA with these kinds of micro-organisms, the family , which includes mainly halophilic bacteria, was chosen as a model. This family comprises ten genera with validly published names and 85 species of environmental, biotechnological and clinical interest. In some cases, the phylogenetic relationships between members of this family, based on 16S rRNA gene sequence comparisons, are not clear and a deep phylogenetic analysis using several housekeeping genes seemed appropriate. Here, MLSA was applied using the 16S rRNA, 23S rRNA, , , and genes for species of the family . Phylogenetic trees based on the individual and concatenated gene sequences revealed that the family formed a monophyletic group of micro-organisms within the order . With the exception of the genera and , all other genera within this family were phylogenetically coherent. Five of the six studied genes (16S rRNA, 23S rRNA, , and ) showed a consistent evolutionary history. However, the results obtained with the gene were different; thus, this gene may not be considered useful as an individual gene phylogenetic marker within this family. The phylogenetic methods produced variable results, with those generated from the maximum-likelihood and neighbour-joining algorithms being more similar than those obtained by maximum-parsimony methods. Horizontal gene transfer (HGT) plays an important evolutionary role in the family ; however, the impact of recombination events in the phylogenetic analysis was minimized by concatenating the six loci, which agreed with the current taxonomic scheme for this family. Finally, the findings of this study also indicated that the 16S rRNA, and genes were the most suitable genes for future taxonomic studies using MLSA within the family .

Funding
This study was supported by the:
  • Spanish Ministerio de Educación y Ciencia
  • Spanish Ministerio de Educación y Ciencia (Award CGL2010-19303 and BIO2009-10138)
  • National Science Foundation (Award 0830024 and DEB-0919290)
  • US–Israel Binational Science Foundation (Award 2007043)
  • Junta de Andalucía (Award P06-CVI-01829)
  • FEDER funds
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2012-03-01
2024-03-29
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References

  1. Ah-You N., Gagnevin L., Grimont P. A. D., Brisse S., Nesme X., Chiroleu F., Bui Thi Ngoc L., Jouen E., Lefeuvre P. other authors 2009; Polyphasic characterization of xanthomonads pathogenic to members of the Anacardiaceae and their relatedness to species of Xanthomonas . Int J Syst Evol Microbiol 59:306–318 [View Article][PubMed]
    [Google Scholar]
  2. Anan’ina L. N., Plotnikova E. G., Gavrish E. Iu., Demakov V. A., Evtushenko L. I. 2007; [Salinicola socius gen. nov., sp. nov., a moderately halophilic bacterium from a naphthalene-utilizing microbial association]. Mikrobiologiia 76:369–376 (English translation of Mikrobiologiia) [PubMed]
    [Google Scholar]
  3. Anisimova M., Gascuel O. 2006; Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55:539–552 [View Article][PubMed]
    [Google Scholar]
  4. Arahal D. R., Ventosa A. 2006; The family Halomonadaceae . In The Prokaryotes, 3rd edn. vol. 6 pp. 811–835 Edited by Dworkin M., Falkow S., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Springer; [CrossRef]
    [Google Scholar]
  5. Arahal D. R., García M. T., Ludwig W., Schleifer K. H., Ventosa A. 2001; Transfer of Halomonas canadensis and Halomonas israelensis to the genus Chromohalobacter as Chromohalobacter canadensis comb. nov. and Chromohalobacter israelensis comb. nov.. Int J Syst Evol Microbiol 51:1443–1448[PubMed]
    [Google Scholar]
  6. Arahal D. R., Castillo A. M., Ludwig W., Schleifer K. H., Ventosa A. 2002a; Proposal of Cobetia marina gen. nov., comb. nov., within the family Halomonadaceae, to include the species Halomonas marina . Syst Appl Microbiol 25:207–211 [View Article][PubMed]
    [Google Scholar]
  7. Arahal D. R., Ludwig W., Schleifer K. H., Ventosa A. 2002b; Phylogeny of the family Halomonadaceae based on 23S and 16S rDNA sequence analyses. Int J Syst Evol Microbiol 52:241–249[PubMed]
    [Google Scholar]
  8. Arahal D. R., Vreeland R. H., Litchfield C. D., Mormile M. R., Tindall B. J., Oren A., Bejar V., Quesada E., Ventosa A. 2007; Recommended minimal standards for describing new taxa of the family Halomonadaceae . Int J Syst Evol Microbiol 57:2436–2446 [View Article][PubMed]
    [Google Scholar]
  9. Baldwin A., Mahenthiralingam E., Thickett K. M., Honeybourne D., Maiden M. C. J., Govan J. R., Speert D. P., Lipuma J. J., Vandamme P., Dowson C. G. 2005; Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 43:4665–4673 [View Article][PubMed]
    [Google Scholar]
  10. Barrett M., Donoghue M. J., Sober E. 1991; Against consensus. Syst Zool 40:486–493 [View Article]
    [Google Scholar]
  11. Ben Ali Gam Z., Abdelkafi S., Casalot L., Tholozan J. L., Oueslati R., Labat M. 2007; Modicisalibacter tunisiensis gen. nov., sp. nov., an aerobic, moderately halophilic bacterium isolated from an oilfield-water injection sample, and emended description of the family Halomonadaceae Franzmann et al. 1989 emend Dobson and Franzmann 1996 emend. Ntougias et al. 2007. Int J Syst Evol Microbiol 57:2307–2313 [View Article][PubMed]
    [Google Scholar]
  12. Blattner F. R., Plunkett G. III, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K. other authors 1997; The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462 [View Article][PubMed]
    [Google Scholar]
  13. Brady C., Cleenwerck I., Venter S., Vancanneyt M., Swings J., Coutinho T. 2008; Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31:447–460 [View Article][PubMed]
    [Google Scholar]
  14. Bull J. J., Huelsenbeck J., Cunningham C. W., Swofford D. L., Waddell P. J. 1993; Partitioning and combining data in phylogenetic analyses. Syst Biol 42:384–397 [CrossRef]
    [Google Scholar]
  15. Christensen H., Bisgaard M., Frederiksen W., Mutters R., Kuhnert P., Olsen J. E. 2001; Is characterization of a single isolate sufficient for valid publication of a new genus or species? Proposal to modify recommendation 30b of the Bacteriological Code (1990 Revision). Int J Syst Evol Microbiol 51:2221–2225 [View Article][PubMed]
    [Google Scholar]
  16. Cladera A. M., Sepúlveda-Torres L. del C., Valens-Vadell M., Meyer J.-M., Lalucat J., García-Valdés E. 2006; A detailed phenotypic and genotypic description of Pseudomonas strain OX1. Syst Appl Microbiol 29:422–430 [View Article][PubMed]
    [Google Scholar]
  17. de la Haba R. R., Arahal D. R., Márquez M. C., Ventosa A. 2010; Phylogenetic relationships within the family Halomonadaceae based on comparative 23S and 16S rRNA gene sequence analysis. Int J Syst Evol Microbiol 60:737–748 [View Article][PubMed]
    [Google Scholar]
  18. Dobson S. J., Franzmann P. D. 1996; Unification of the genera Deleya (Baumann et al. 1983), Halomonas (Vreeland et al. 1980), and Halovibrio (Fendrich 1988) and the species Paracoccus halodenitrificans (Robinson and Gibbons 1952) into a single genus, Halomonas, and placement of the genus Zymobacter in the family Halomonadaceae . Int J Syst Bacteriol 46:550–558 [View Article]
    [Google Scholar]
  19. Euzéby J. P. 2010 List of Prokaryotic names with Standing in Nomenclature http://www.bacterio.cict.fr
  20. Felsenstein J. 1981; Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376 [View Article][PubMed]
    [Google Scholar]
  21. Franzmann P. D., Wehmeyer U., Stackerbrandt E. 1988; Halomonadaceae fam. nov., a new family of the class Proteobacteria to accommodate the genera Halomonas and Deleya . Syst Appl Microbiol 11:16–19 [CrossRef]
    [Google Scholar]
  22. Garriga M., Ehrmann M. A., Arnau J., Hugas M., Vogel R. F. 1998; Carnimonas nigrificans gen. nov., sp. nov., a bacterial causative agent for black spot formation on cured meat products. Int J Syst Bacteriol 48:677–686 [View Article][PubMed]
    [Google Scholar]
  23. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  24. Hanage W. P., Kaijalainen T., Herva E., Saukkoriipi A., Syrjänen R., Spratt B. G. 2005; Using multilocus sequence data to define the pneumococcus. J Bacteriol 187:6223–6230 [View Article][PubMed]
    [Google Scholar]
  25. Hodgetts J., Boonham N., Mumford R., Harrison N., Dickinson M. 2008; Phytoplasma phylogenetics based on analysis of secA and 23S rRNA gene sequences for improved resolution of candidate species of ‘Candidatus Phytoplasma’. Int J Syst Evol Microbiol 58:1826–1837 [View Article][PubMed]
    [Google Scholar]
  26. Ivars-Martínez E., D’Auria G., Rodríguez-Valera F., Sânchez-Porro C., Ventosa A., Joint I., Mühling M. 2008; Biogeography of the ubiquitous marine bacterium Alteromonas macleodii determined by multilocus sequence analysis. Mol Ecol 17:4092–4106 [View Article][PubMed]
    [Google Scholar]
  27. Jeong H., Yim J. H., Lee C., Choi S. H., Park Y. K., Yoon S. H., Hur C. G., Kang H. Y., Kim D. other authors 2005; Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucleic Acids Res 33:7066–7073 [View Article][PubMed]
    [Google Scholar]
  28. Kim K. K., Lee K. C., Oh H.-M., Lee J.-S. 2010; Halomonas stevensii sp. nov., Halomonas hamiltonii sp. nov. and Halomonas johnsoniae sp. nov., isolated from a renal care centre. Int J Syst Evol Microbiol 60:369–377 [View Article][PubMed]
    [Google Scholar]
  29. Kishino H., Hasegawa M. 1989; Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29:170–179 [View Article][PubMed]
    [Google Scholar]
  30. Kluge A. G. 1989; A concern for evidence and phylogenetic hypothesis relationships among Epicrates (Boidae, Serpentes). Syst Zool 38:7–25 [View Article]
    [Google Scholar]
  31. Kluge A. G., Farris J. S. 1969; Quantitative phyletics and the evolution of anurans. Syst Zool 18:1–32 [View Article]
    [Google Scholar]
  32. Küpfer M., Kuhnert P., Korczak B. M., Peduzzi R., Demarta A. 2006; Genetic relationships of Aeromonas strains inferred from 16S rRNA, gyrB and rpoB gene sequences. Int J Syst Evol Microbiol 56:2743–2751 [View Article][PubMed]
    [Google Scholar]
  33. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. other authors 2007; Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  34. Lee J.-C., Jeon C. O., Lim J.-M., Lee S.-M., Lee J.-M., Song S.-M., Park D.-J., Li W.-J., Kim C.-J. 2005; Halomonas taeanensis sp. nov., a novel moderately halophilic bacterium isolated from a solar saltern in Korea. Int J Syst Evol Microbiol 55:2027–2032 [View Article][PubMed]
    [Google Scholar]
  35. Maddison D. R., Maddison W. P. 2000 MacClade 4: Analysis of Phylogeny and Character Evolution, version 4.0 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  36. Martens M., Delaere M., Coopman R., De Vos P., Gillis M., Willems A. 2007; Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57:489–503 [View Article][PubMed]
    [Google Scholar]
  37. Martens M., Dawyndt P., Coopman R., Gillis M., De Vos P., Willems A. 2008; Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214 [View Article][PubMed]
    [Google Scholar]
  38. Martínez-Cánovas M. J., Quesada E., Llamas I., Béjar V. 2004; Halomonas ventosae sp. nov., a moderately halophilic, denitrifying, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 54:733–737 [View Article][PubMed]
    [Google Scholar]
  39. Miyamoto M. M., Fitch W. M. 1995; Testing species phylogenies and phylogenetic methods with congruence. Syst Biol 44:64–76 [CrossRef]
    [Google Scholar]
  40. Ntougias S., Zervakis G. I., Fasseas C. 2007; Halotalea alkalilenta gen. nov., sp. nov., a novel osmotolerant and alkalitolerant bacterium from alkaline olive mill wastes, and emended description of the family Halomonadaceae Franzmann et al. 1989, emend. Dobson and Franzmann 1996. Int J Syst Evol Microbiol 57:1975–1983 [View Article][PubMed]
    [Google Scholar]
  41. Okamoto T., Taguchi H., Nakamura K., Ikenaga H., Kuraishi H., Yamasato K. 1993; Zymobacter palmae gen. nov., sp. nov., a new ethanol-fermenting peritrichous bacterium isolated from palm sap. Arch Microbiol 160:333–337 [View Article][PubMed]
    [Google Scholar]
  42. Okamoto T., Maruyama A., Imura S., Takeyama H., Naganuma T. 2004; Comparative phylogenetic analyses of Halomonas variabilis and related organisms based on 16S rRNA, gyrB and ectBC gene sequences. Syst Appl Microbiol 27:323–333 [View Article][PubMed]
    [Google Scholar]
  43. Pascual J., Macián M. C., Arahal D. R., Garay E., Pujalte M. J. 2010; Multilocus sequence analysis of the central clade of the genus Vibrio by using the 16S rRNA, recA, pyrH, rpoD, gyrB, rctB and toxR genes. Int J Syst Evol Microbiol 60:154–165 [View Article][PubMed]
    [Google Scholar]
  44. Riley M., Abe T., Arnaud M. B., Berlyn M. K., Blattner F. R., Chaudhuri R. R., Glasner J. D., Horiuchi T., Keseler I. M. other authors 2006; Escherichia coli K-12: a cooperatively developed annotation snapshot – 2005. Nucleic Acids Res 34:1–9 [View Article][PubMed]
    [Google Scholar]
  45. Rosselló-Mora R. 2006; DNA-DNA reassociation methods applied to microbial taxonomy and their critical evaluation. In Molecular Identification, Systematics and Population Structure of Prokaryotes pp. 23–50 Edited by Stackebrandt E. Heidelberg: Springer; [View Article]
    [Google Scholar]
  46. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  47. Sánchez-Porro C., de la Haba R. R., Soto-Ramírez N., Márquez M. C., Montalvo-Rodríguez R., Ventosa A. 2009; Description of Kushneria aurantia gen. nov., sp. nov., a novel member of the family Halomonadaceae, and a proposal for reclassification of Halomonas marisflavi as Kushneria marisflavi comb. nov., of Halomonas indalinina as Kushneria indalinina comb. nov. and of Halomonas avicenniae as Kushneria avicenniae comb. nov.. Int J Syst Evol Microbiol 59:397–405 [View Article][PubMed]
    [Google Scholar]
  48. Schneiker S., Martins dos Santos V. A., Bartels D., Bekel T., Brecht M., Buhrmester J., Chernikova T. N., Denaro R., Ferrer M. other authors 2006; Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis . Nat Biotechnol 24:997–1004 [View Article][PubMed]
    [Google Scholar]
  49. Seshadri R., Joseph S. W., Chopra A. K., Sha J., Shaw J., Graf J., Haft D., Wu M., Ren Q. other authors 2006; Genome sequence of Aeromonas hydrophila ATCC 7966T: jack of all trades. J Bacteriol 188:8272–8282 [View Article][PubMed]
    [Google Scholar]
  50. Sheppard S. K., McCarthy N. D., Falush D., Maiden M. C. 2008; Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237–239 [View Article][PubMed]
    [Google Scholar]
  51. Shimodaira H., Hasegawa M. 1999; Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116 [CrossRef]
    [Google Scholar]
  52. Soler L., Yáñez M. A., Chacon M. R., Aguilera-Arreola M. G., Catalán V., Figueras M. J., Martínez-Murcia A. J. 2004; Phylogenetic analysis of the genus Aeromonas based on two housekeeping genes. Int J Syst Evol Microbiol 54:1511–1519 [View Article][PubMed]
    [Google Scholar]
  53. Stackebrandt E., Frederiksen W., Garrity G. M., Grimont P. A. D., Kämpfer P., Maiden M. C. J., Nesme X., Rosselló-Mora R., Swings J. other authors 2002; Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047 [View Article][PubMed]
    [Google Scholar]
  54. Stevens D. A., Hamilton J. R., Johnson N., Kim K. K., Lee J. S. 2009; Halomonas, a newly recognized human pathogen causing infections and contamination in a dialysis center: three new species. Medicine (Baltimore) 88:244–249 [View Article][PubMed]
    [Google Scholar]
  55. Stover C. K., Pham X. Q., Erwin A. L., Mizoguchi S. D., Warrener P., Hickey M. J., Brinkman F. S., Hufnagle W. O., Kowalik D. J. other authors 2000; Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964 [View Article][PubMed]
    [Google Scholar]
  56. Swofford D. L. 2002; paup*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates;
  57. Tavaré S. 1986; Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci 17:57–86
    [Google Scholar]
  58. Thompson C. C., Thompson F. L., Vicente A. C. P., Swings J. 2007; Phylogenetic analysis of vibrios and related species by means of atpA gene sequences. Int J Syst Evol Microbiol 57:2480–2484 [View Article][PubMed]
    [Google Scholar]
  59. Tindall B. J., Rosselló-Móra R., Busse H.-J., Ludwig W., Kämpfer P. 2010; Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266 [View Article][PubMed]
    [Google Scholar]
  60. Ventosa A., Quesada E., Rodriguez-Valera F., Ruiz-Berraquero F., Ramos-Cormenzana A. 1982; Numerical taxonomy of moderately halophilic Gram-negative rods. J Gen Microbiol 128:1959–1968
    [Google Scholar]
  61. Ventosa A., Gutiérrez M. C., García M. T., Ruiz-Berraquero F. 1989; Classification of “Chromobacterium marismortui” in a new genus, Chromohalobacter gen. nov., as Chromohalobacter marismortui comb. nov., nom. rev.. Int J Syst Bacteriol 39:382–386 [View Article]
    [Google Scholar]
  62. von Graevenitz A., Bowman J., Del Notaro C., Ritzler M. 2000; Human infection with Halomonas venusta following fish bite. J Clin Microbiol 38:3123–3124[PubMed]
    [Google Scholar]
  63. Vreeland R. H., Litchfield C. D., Martin E. L., Elliot E. 1980; Halomonas elongata, a new genus and species of extremely salt-tolerant bacteria. Int J Syst Bacteriol 30:485–495 [View Article]
    [Google Scholar]
  64. Wang Y., Tang S.-K., Lou K., Lee J.-C., Jeon C. O., Xu L.-H., Kim C.-J., Li W.-J. 2009; Aidingimonas halophila gen. nov., sp. nov., a moderately halophilic bacterium isolated from a salt lake. Int J Syst Evol Microbiol 59:3088–3094 [View Article][PubMed]
    [Google Scholar]
  65. Wolfe-Simon F., Switzer Blum J., Kulp T. R., Gordon G. W., Hoeft S. E., Pett-Ridge J., Stolz J. F., Webb S. M., Weber P. K. other authors 2011; A bacterium that can grow by using arsenic instead of phosphorus. Science 332:1163–1166[PubMed] [CrossRef]
    [Google Scholar]
  66. Yoon J.-H., Lee K.-C., Kho Y. H., Kang K. H., Kim C.-J., Park Y.-H. 2002; Halomonas alimentaria sp. nov., isolated from jeotgal, a traditional Korean fermented seafood. Int J Syst Evol Microbiol 52:123–130[PubMed] [CrossRef]
    [Google Scholar]
  67. 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 [View Article][PubMed]
    [Google Scholar]
  68. Zeigler D. R. 2003; Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Evol Microbiol 53:1893–1900 [View Article][PubMed]
    [Google Scholar]
  69. Zhaxybayeva O., Doolittle W. F., Papke R. T., Gogarten J. P. 2009; Intertwined evolutionary histories of marine Synechococcus and Prochlorococcus marinus . Genome Biol Evol 1:325–339 [View Article][PubMed]
    [Google Scholar]
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