1887

Abstract

We used the information from a set of concatenated sequences from four genes (, , and ) to investigate the phylogeny of the genera and (entomopathogenic bacteria associated with nematodes of the genera and , respectively). The robustness of the phylogenetic tree obtained by this multigene approach was significantly better than that of the tree obtained by a single gene approach. The comparison of the topologies of single gene phylogenetic trees highlighted discrepancies which have implications for the classification of strains and new isolates; in particular, we propose the transfer of subsp. to subsp. comb. nov. (type strain CIP 108426 =DSM 15199). We found that, within the genus , strains or isolates that shared less than 97 % nucleotide identity (NI), calculated on the concatenated sequences of the four gene fragments (, , and ) encompassing 3395 nucleotides, did not belong to the same species. Thus, at the 97 % NI cutoff, we confirm the current 20 species of the genus and propose the description of a novel species, sp. nov. (type strain VN01 = CIP 109945 =DSM 22392). Within each of the three current species of the genus , , and , strains or isolates which shared less than 97 % NI did not belong to the same subspecies. Comparisons of the four gene fragments plus the gene fragment analysed separately led us to propose four novel subspecies: subsp. subsp. nov. (type strain HG29 =CIP 109949 =DSM 22391), subsp. subsp. nov. (type strain C8404 = CIP 109946 =DSM 22397), subsp. subsp. nov. (type strain C1 =NC19 =CIP 109947 =DSM 3369), and subsp. subsp. nov. (type strain T327 = CIP 109948 =DSM 22387).

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2010-08-01
2019-12-13
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References

  1. Akhurst, R. J. & Boemare, N. E. ( 1988; ). A numerical taxonomic study of the genus Xenorhabdus (Enterobacteriaceae) and proposed elevation of the subspecies of X. nematophilus to species. J Gen Microbiol 134, 1835–1845.
    [Google Scholar]
  2. Akhurst, R. J., Mourant, R. G., Baud, L. & Boemare, N. E. ( 1996; ). Phenotypic and DNA relatedness between nematode symbionts and clinical strains of the genus Photorhabdus (Enterobacteriaceae). Int J Syst Bacteriol 46, 1034–1041.[CrossRef]
    [Google Scholar]
  3. Akhurst, R. J., Boemare, N. E., Janssen, P. H., Peel, M. M., Alfredson, D. A. & Beard, C. E. ( 2004; ). Taxonomy of Australian clinical isolates of the genus Photorhabdus and proposal of subspecies Photorhabdus asymbiotica subsp. asymbiotica subsp. nov. and Photorhabdus asymbiotica subsp. australis subsp. nov. Int J Syst Evol Microbiol 54, 1301–1310.[CrossRef]
    [Google Scholar]
  4. Bleakley, B. & Nealson, K. H. ( 1988; ). Characterization of primary and secondary forms of Xenorhabdus luminescens strain Hm. FEMS Microbiol Lett 53, 241–250.
    [Google Scholar]
  5. Boemare, N. E. & Akhurst, R. J. ( 1988; ). Biochemical and physiological characterization of colony form variants in Xenorhabdus spp. (Enterobacteriaceae). J Gen Microbiol 134, 751–761.
    [Google Scholar]
  6. Boemare, N. E., Akhurst, R. J. & Mourant, R. G. ( 1993; ). DNA relatedness between Xenorhabdus spp. (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen. nov. Int J Syst Bacteriol 43, 249–255.[CrossRef]
    [Google Scholar]
  7. Brunel, B., Givaudan, A., Lanois, A., Akhurst, R. J. & Boemare, N. ( 1997; ). Fast and accurate identification of Xenorhabdus and Photorhabdus species by restriction analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 63, 574–580.
    [Google Scholar]
  8. Dewhirst, F. E., Shen, Z., Scimeca, M. S., Stokes, L. N., Boumenna, T., Chen, T., Paster, B. J. & Fox, J. G. ( 2005; ). Discordant 16S and 23S rRNA gene phylogenies for the genus Helicobacter: implications for phylogenetic inference and systematics. J Bacteriol 187, 6106–6118.[CrossRef]
    [Google Scholar]
  9. Doolittle, W. F. ( 1999; ). Lateral genomics. Trends Cell Biol 9, M5–M9.[CrossRef]
    [Google Scholar]
  10. Eardly, B. D., Wang, F.-S. & van Berkum, P. ( 1996; ). Corresponding 16S rRNA gene segments in Rhizobiaceae and Aeromonas yield discordant phylogenies. Plant Soil 186, 69–74.[CrossRef]
    [Google Scholar]
  11. Eisen, J. A. ( 1995; ). The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol 41, 1105–1123.
    [Google Scholar]
  12. Emelianoff, V., Le Brun, N., Pagès, S., Stock, S. P., Tailliez, P., Moulia, C. & Sicard, M. ( 2008; ). Isolation and identification of entomopathogenic nematodes and their symbiotic bacteria from Hérault and Gard (Southern France). J Invertebr Pathol 98, 211–217.[CrossRef]
    [Google Scholar]
  13. Felsenstein, J. ( 1988; ). Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22, 521–565.[CrossRef]
    [Google Scholar]
  14. Fischer-Le Saux, M., Mauléon, H., Constant, P., Brunel, B. & Boemare, N. ( 1998; ). PCR-ribotyping of Xenorhabdus and Photorhabdus isolates from the Caribbean region in relation to the taxonomy and geographic distribution of their nematode hosts. Appl Environ Microbiol 64, 4246–4254.
    [Google Scholar]
  15. Fischer-Le Saux, M., Viallard, V., Brunel, B., Normand, P. & Boemare, N. E. ( 1999; ). Polyphasic classification of the genus Photorhabdus and proposal of new taxa: P. luminescens subsp. luminescens subsp. nov., P. luminescens subsp. akhurstii subsp. nov., P. luminescens subsp. laumondii subsp. nov., P. temperata sp. nov., P. temperata subsp. temperata subsp. nov. and P. asymbiotica sp. nov. Int J Syst Bacteriol 49, 1645–1656.[CrossRef]
    [Google Scholar]
  16. Gevers, D., Cohan, F. M., Lawrence, J. G., Spratt, B. G., Coenye, T., Feil, E. J., Stackebrandt, E., Van de Peer, Y., Vandamme, P. & other authors ( 2005; ). Re-evaluating prokaryotic species. Nat Rev Microbiol 3, 733–739.[CrossRef]
    [Google Scholar]
  17. Hannula, M. & Hänninen, M.-L. ( 2007; ). Phylogenetic analysis of Helicobacter species based on partial gyrB gene sequences. Int J Syst Evol Microbiol 57, 444–449.[CrossRef]
    [Google Scholar]
  18. Hazir, S., Stackebrandt, E., Lang, E., Schumann, P., Ehlers, R. U. & Keskin, N. ( 2004; ). Two new subspecies of Photorhabdus luminescens, isolated from Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae): Photorhabdus luminescens subsp. kayaii subsp. nov. and Photorhabdus luminescens subsp. thracensis subsp. nov. Syst Appl Microbiol 27, 36–42.[CrossRef]
    [Google Scholar]
  19. Jain, R., Rivera, M. C. & Lake, J. A. ( 1999; ). Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96, 3801–3806.[CrossRef]
    [Google Scholar]
  20. Jolley, K. A., Feil, E. J., Chan, M.-S. & Maiden, M. C. J. ( 2001; ). Sequence type analysis and recombinational tests (START). Bioinformatics 17, 1230–1231.[CrossRef]
    [Google Scholar]
  21. Khan, A., Brooks, W. M. & Hirschmann, H. ( 1976; ). Chromonema heliothidis n. gen., s. sp. (Steinernematidae, Nematoda), a parasite of Heliothis zea (Noctuidae, Lepidoptera), and other insects. J Nematol 8, 159–168.
    [Google Scholar]
  22. Kimura, M. ( 1980; ). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16, 111–120.[CrossRef]
    [Google Scholar]
  23. Kuwata, R., Yoshiga, T., Yoshida, M. & Kondo, E. ( 2008; ). Mutualistic association of Photorhabdus asymbiotica with Japanese heterorhabditid entomopathogenic nematodes. Microbes Infect 10, 734–741.[CrossRef]
    [Google Scholar]
  24. Lengyel, K., Lang, E., Fodor, A., Szállás, E., Schumann, P. & Stackebrandt, E. ( 2005; ). Description of four novel species of Xenorhabdus, family Enterobacteriaceae: Xenorhabdus budapestensis sp. nov., Xenorhabdus ehlersii sp. nov. Xenorhabdus innexi sp. nov., and Xenorhabdus szentirmaii sp. nov. Syst Appl Microbiol 28, 115–122.[CrossRef]
    [Google Scholar]
  25. Lerat, E., Daubin, V. & Moran, N. A. ( 2003; ). From gene trees to organismal phylogeny in prokaryotes: the case of the γ-proteobacteria. PLoS Biol 1, E19
    [Google Scholar]
  26. Marokhazi, J., Waterfield, N., LeGoff, G., Feil, E., Stabler, R., Hinds, J., Fodor, A. & ffrench-Constant, R. H. ( 2003; ). Using a DNA microarray to investigate the distribution of insect virulence factors in strains of Photorhabdus bacteria. J Bacteriol 185, 4648–4656.[CrossRef]
    [Google Scholar]
  27. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
    [Google Scholar]
  28. Parkinson, N., Aritua, V., Heeney, J., Cowie, C., Bew, J. & Stead, D. ( 2007; ). Phylogenetic analysis of Xanthomonas species by comparison of partial gyrase B gene sequences. Int J Syst Evol Microbiol 57, 2881–2887.[CrossRef]
    [Google Scholar]
  29. Phan, K. L., Nguyen, N. C. & Moens, M. ( 2001; ). Steinernema sangi sp. n. (Rhabditida: Steinernematidae) from Vietnam. Russ J Nematol 9, 1–7.
    [Google Scholar]
  30. Poinar, G. O., Jr ( 1975; ). Description and biology of a new insect parasitic rhabditoid, Heterorhabditis bacteriophora n. gen., n. sp. (Rhabditida; Heterorhabditidae n. fam.). Nematologica 21, 463–470.[CrossRef]
    [Google Scholar]
  31. Poinar, G. O., Jr ( 1993; ). Origins and phylogenetic relationships of the entomophilic rhabditids, Heterorhabditis and Steinernema. Fundam Appl Nematol 16, 333–338.
    [Google Scholar]
  32. Poinar, G. O., Jr, Thomas, G. M. & Hess, R. ( 1977; ). Characteristics of the specific bacterium associated with Heterorhabditis bacteriophora (Heterorhabditidae: Rhabditida). Nematologica 23, 97–102.[CrossRef]
    [Google Scholar]
  33. Rainey, F. A., Ehlers, R. U. & Stackebrandt, E. ( 1995; ). Inability of the polyphasic approach to systematics to determine the relatedness of the genera Xenorhabdus and Photorhabdus. Int J Syst Bacteriol 45, 379–381.[CrossRef]
    [Google Scholar]
  34. Rokas, A., Williams, B. L., King, N. & Carroll, S. B. ( 2003; ). Genome-scale approaches to resolving incongruence in molecular phylogenis. Nature 425, 798–804.[CrossRef]
    [Google Scholar]
  35. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  36. Sawyer, S. A. ( 1989; ). Statistical tests for detecting gene conversion. Mol Biol Evol 6, 526–538.
    [Google Scholar]
  37. Schouls, L. M., Schot, C. S. & Jacobs, J. A. ( 2003; ). Horizontal transfer of segments of the 16S rRNA genes between species of the Streptococcus anginosus group. J Bacteriol 185, 7241–7246.[CrossRef]
    [Google Scholar]
  38. Sergeant, M., Baxter, L., Jarrett, P., Shaw, E., Ousley, M., Winstanley, C. & Morgan, J. A. W. ( 2006; ). Identification, typing, and insecticidal activity of Xenorhabdus isolates from entomopathogenic nematodes in United Kingdom soil and characterization of the xpt toxin loci. Appl Environ Microbiol 72, 5895–5907.[CrossRef]
    [Google Scholar]
  39. Sneath, P. H. A. ( 1993; ). Evidence from Aeromonas for genetic crossing-over in ribosomal sequences. Int J Syst Bacteriol 43, 626–629.[CrossRef]
    [Google Scholar]
  40. Somvanshi, V. S., Lang, E., Ganguly, S., Swiderski, J., Saxena, A. K. & Stackebrandt, E. ( 2006; ). A novel species of Xenorhabdus, family enterobacteriaceae: Xenorhabdus indica sp. nov., symbiotically associated with entomopathogenic nematode Steinernema thermophilum Ganguly and Singh, 2000. Syst Appl Microbiol 29, 519–525.[CrossRef]
    [Google Scholar]
  41. Suzuki, T., Yabusaki, H. & Nishimura, Y. ( 1996; ). Phylogenetic relationships of entomopathogenic nematophilic bacteria: Xenorhabdus spp. and Photorhabdus sp. J Basic Microbiol 36, 351–354.[CrossRef]
    [Google Scholar]
  42. Swofford, D. L. ( 2003; ). paup*: Phylogenetic analysis using parsimony (and other methods), version 4.0b10. Sunderland, MA: Sinauer Associates.
  43. Tailliez, P., Pagès, S., Ginibre, N. & Boemare, N. ( 2006; ). New insight into diversity in the genus Xenorhabdus, including the description of ten new species. Int J Syst Evol Microbiol 56, 2805–2818.[CrossRef]
    [Google Scholar]
  44. Thompson, C. C., Thompson, F. L., Vandemeulebroecke, K., Hoste, B., Dawyndt, P. & Swings, J. ( 2004; ). Use of recA as an alternative phylogenetic marker in the family Vibrionaceae. Int J Syst Evol Microbiol 54, 919–924.[CrossRef]
    [Google Scholar]
  45. Tóth, T. & Lakatos, T. ( 2008; ). Photorhabdus temperata subsp. cinerea subsp. nov., isolated from Heterorhabditis nematodes. Int J Syst Evol Microbiol 58, 2579–2581.[CrossRef]
    [Google Scholar]
  46. van Berkum, P., Terefework, Z., Paulin, L., Suomalainen, S., Lindström, K. & Eardly, B. D. ( 2003; ). Discordant phylogenies within the rrn loci of Rhizobia. J Bacteriol 185, 2988–2998.[CrossRef]
    [Google Scholar]
  47. Wang, Y. & Zhang, Z. ( 2000; ). Comparative sequence analyses reveal frequent occurrence of short segments containing an abnormally high number of non-random base variations in bacterial rRNA genes. Microbiology 146, 2845–2854.
    [Google Scholar]
  48. Wang, L.-T., Lee, F.-L., Tai, C.-J. & Kasai, H. ( 2007; ). Comparison of gyrB gene sequences, 16S rRNA gene sequences and DNA-DNA hybridization in the Bacillus subtilis group. Int J Syst Evol Microbiol 57, 1846–1850.[CrossRef]
    [Google Scholar]
  49. Wayne, L. G., Brenner, D. J., Colwell, R. R., Grimont, P. A. D., Kandler, O., Krichevsky, M. I., Moore, L. H., Moore, W. E. C., Murray, R. G. E. & other authors ( 1987; ). International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37, 463–464.[CrossRef]
    [Google Scholar]
  50. Wertz, J. E., Goldstone, C., Gordon, D. M. & Riley, M. A. ( 2003; ). A molecular phylogeny of enteric bacteria and implications for bacterial species concept. J Evol Biol 16, 1236–1248.[CrossRef]
    [Google Scholar]
  51. Yap, W. H., Zhang, Z. & Wang, Y. ( 1999; ). Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol 181, 5201–5209.
    [Google Scholar]
  52. Yarza, P., Richter, M., Peplies, J., Euzeby, J., Amann, R., Schleifer, K.-H., Ludwig, W., Glöckner, F. O. & Rosselló-Móra, R. ( 2008; ). The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31, 241–250.[CrossRef]
    [Google Scholar]
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