1887

Abstract

Bacterial symbionts are crucial for the infectivity and success of entomopathogenic nematodes as biological control agents. The current understanding of the symbiotic relationships is limited by taxonomic uncertainties. Here, we used whole-genome sequencing and traditional techniques to reconstruct the phylogenetic relationships between all described Photorhabdus species and subspecies as well as 11 newly isolated symbiotic bacteria of Heterorhabditis nematodes, including the unreported bacterial partner of H. beicherriana. In silico DNA–DNA hybridization, orthologous average nucleotide identity and nucleotide sequence identity of concatenated housekeeping genes scores were calculated and set into relation with current cut-off values for species delimitation in bacteria. Sequence data were complemented with biochemical and chemotaxonomic markers, and ribosomal protein fingerprinting profiles. This polyphasic approach resolves the ambiguous taxonomy of Photorhabdus and lead to the proposal for the elevation of most of them into a higher taxon and the creation of several new taxa: 15 new species, one of which is newly described: Photorhabdus bodei sp. nov. (type strain LJ24-63=DSM 105690=CCOS 1159) and the other 14 arise through the proposal of elevating already described subspecies to species, and are proposed to be renamed as follows: Photorhabdus asymbiotica subsp. australis as Photorhabdus australis sp. nov., Photorhabdus luminescens subsp. akhurstii as Photorhabdus akhurstii sp. nov., Photorhabdus luminescens subsp. caribbeanensis as Photorhabdus caribbeanensis sp. nov., Photorhabdus luminescens subsp. hainanensis as Photorhabdus hainanensis sp. nov., Photorhabdus luminescens subsp. kayaii as Photorhabdus kayaii sp. nov., Photorhabdus luminescens subsp. kleinii as Photorhabdus kleinii sp. nov., Photorhabdus luminescens subsp. namnaonensis as Photorhabdus namnaonensis sp. nov., Photorhabdus luminescens subsp. noenieputensis as Photorhabdus noenieputensis sp. nov., Photorhabdus luminescens subsp. laumondii as Photorhabdus laumondii sp. nov., Photorhabdus temperata subsp. cinerea as Photorhabdus cinerea sp. nov., Photorhabdus temperata subsp. khanii as Photorhabdus khanii sp. nov., Photorhabdus temperata subsp. stackebrandtii as Photorhabdus stackebrandtii sp. nov., Photorhabdus temperata subsp. tasmaniensis as Photorhabdus tasmaniensis sp. nov., and Photorhabdus temperata subsp. thracensis as Photorhabdus thracensis sp. nov. In addition, we propose the creation of two new subspecies, one of which arises through the reduction of rank: Photorhabdus laumondii subsp. laumondii comb. nov. (basonym: P. luminescens subsp. laumondii ) and the second one is newly described: Photorhabdus laumondii subsp. clarkei subsp. nov. (type strain BOJ-47=DSM 105531=CCOS 1160). Finally, we propose to emend the description of three species, which results from the proposal of elevating three subspecies to the species status: Photorhabdus asymbiotica , Photorhabdus temperata and Photorhabdus luminescens , formerly classified as Photorhabdus asymbiotica subsp. asymbiotica , Photorhabdus temperata subsp. temperata and Photorhabdus luminescens subsp. luminescens , respectively.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002820
2018-06-07
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/68/8/2664.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002820&mimeType=html&fmt=ahah

References

  1. Kaya HK. Soil ecology. In Gaugler R, Kaya HK. (editors) Entomopathogenic Nematodes in Biological Control Boca Ratón, FL: CRC Press; 1990 pp. 92–115
    [Google Scholar]
  2. Lacey LA, Georgis R. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. J Nematol 2012; 44:218[PubMed]
    [Google Scholar]
  3. Poinar GO, Veremchuk GV. A new strain of entomopathogenic nematode and geographical distribution of Neoaplectana carpocapsae Weiser (Rhabditida, Steinernematidae). Zool Zhurnal 1970; 49:966–969
    [Google Scholar]
  4. Khan A, Brooks WM, Hirschmann H. Chromonema heliothidis n. gen., n. sp. (Steinernematidae, Nematoda), a parasite of Heliothis zea (Noctuidae, Lepidoptera), and other insects. J Nematol 1976; 8:159[PubMed]
    [Google Scholar]
  5. Thomas GM, Poinar GO. Xenorhabdus gen. nov., a genus of entomopathogenic, nematophilic bacteria of the family Enterobacteriaceae. Int J Syst Evol Microbiol 1979; 29:352–360 [View Article]
    [Google Scholar]
  6. Boemare NE, Akhurst RJ, Mourant RG. 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 Evol Microbiol 1993; 43:249–255 [View Article]
    [Google Scholar]
  7. Kaya HK, Gaugler R. Entomopathogenic nematodes. Annu Rev Entomol 1993; 38:181–206 [View Article]
    [Google Scholar]
  8. Sohlenius B. Abundance, biomass and contribution to energy flow by soil nematodes in Terrestrial ecosystems. Oikos 1980; 34:186–194 [View Article]
    [Google Scholar]
  9. Campos-Herrera R, Johnson EG, El-Borai FE, Stuart RJ, Graham JH et al. Long-term stability of entomopathogenic nematode spatial patterns in soil as measured by sentinel insects and real-time PCR assays. Ann Appl Biol 2011; 158:55–68 [View Article]
    [Google Scholar]
  10. Hiltpold I. Prospects in the application technology and formulation of entomopathogenic nematodes for biological control of insect pests. In Campos-Herrera R. (editor) Nematode Pathogenesis of Insects and Other Pests Cham, Germany: Springer Press; 2015 pp. 187–205
    [Google Scholar]
  11. Stuart RJ, Barbercheck ME, Grewal PS. Entomopathogenic nematodes in the soil environment: distributions, interactions and the influence of biotic and abiotic factors. In Campos-Herrera R. (editor) Nematode Pathogenesis of Insects and Other Pests Cham, Germany: Springer Press; 2015 pp. 97–137
    [Google Scholar]
  12. Smart GC. Entomopathogenic nematodes for the biological control of insects. J Nematol 1995; 27:529[PubMed]
    [Google Scholar]
  13. Grewal PS, Ehlers RU, Shapiro-Ilan DI. Nematodes as biocontrol agents. In Grewal PS, Ehlers RU, Shapiro-Ilan DI. (editors) Nematodes as Biocontrol Agents Wallingford, UK: CABI Publishing Group; 2005 pp. 1–513
    [Google Scholar]
  14. Denno RF, Gruner DS, Kaplan I. Potential for entomopathogenic nematodes in biological control: a meta-analytical synthesis and insights from trophic cascade theory. J Nematol 2008; 40:61[PubMed]
    [Google Scholar]
  15. Xing-Yue L, Qi-Zhi L, Nermut J, Puza V, Mracek Z. Heterorhabditis beicherriana n. sp. (Nematoda: Heterorhabditidae), a new entomopathogenic nematode from the Shunyi district of Beijing, China. Zootaxa 2012; 3569:25–40
    [Google Scholar]
  16. Hunt DJ, Nguyen KB. Advances in entomopathogenic nematode taxonomy and phylogeny. In Hunt DJ, Nguyen KB. (editors) Advances in Entomopathogenic Nematode Taxonomy and Phylogeny Leiden, Netherlands: Brill; 2016 pp. 1–403
    [Google Scholar]
  17. Peat SM, Ffrench-Constant RH, Waterfield NR, Marokházi J, Fodor A et al. A robust phylogenetic framework for the bacterial genus Photorhabdus and its use in studying the evolution and maintenance of bioluminescence: a case for 16S, gyrB, and glnA. Mol Phylogenet Evol 2010; 57:728–740 [View Article][PubMed]
    [Google Scholar]
  18. Fischer-Le Saux M, Viallard V, Brunel B, Normand P, Boemare NE. 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 Evol Microbiol 1999; 49:1645–1656 [View Article][PubMed]
    [Google Scholar]
  19. Akhurst RJ, Boemare NE, Janssen PH, Peel MM, Alfredson DA et al. Taxonomy of Australian clinical isolates of the genus Photorhabdus and proposal of Photorhabdus asymbiotica subsp. asymbiotica subsp. nov. and P. asymbiotica subsp. australis subsp. nov. Int J Syst Evol Microbiol 2004; 54:1301–1310 [View Article][PubMed]
    [Google Scholar]
  20. Szállás E, Koch C, Fodor A, Burghardt J, Buss O et al. Phylogenetic evidence for the taxonomic heterogeneity of Photorhabdus luminescens. Int J Syst Evol Microbiol 1997; 47:402–407 [View Article][PubMed]
    [Google Scholar]
  21. Hazir S, Stackebrandt E, Lang E, Schumann P, Ehlers RU et al. 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 2004; 27:36–42 [View Article][PubMed]
    [Google Scholar]
  22. Tóth T, Lakatos T. Photorhabdus temperata subsp. cinerea subsp. nov., isolated from Heterorhabditis nematodes. Int J Syst Evol Microbiol 2008; 58:2579–2581 [View Article][PubMed]
    [Google Scholar]
  23. An R, Grewal PS. Photorhabdus luminescens subsp. kleinii subsp. nov. (Enterobacteriales: Enterobacteriaceae). Curr Microbiol 2011; 62:539–543 [View Article][PubMed]
    [Google Scholar]
  24. An R, Grewal PS. Photorhabdus temperata subsp. stackebrandtii subsp. nov. (Enterobacteriales: Enterobacteriaceae). Curr Microbiol 2010; 61:291–297 [View Article][PubMed]
    [Google Scholar]
  25. Tailliez P, Laroui C, Ginibre N, Paule A, Pagès S et al. Phylogeny of Photorhabdus and Xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. vietnamensis sp. nov., P. luminescens subsp. caribbeanensis subsp. nov., P. luminescens subsp. hainanensis subsp. nov., P. temperata subsp. khanii subsp. nov., P. temperata subsp. tasmaniensis subsp. nov., and the reclassification of P. luminescens subsp. thracensis as P. temperata subsp. thracensis comb. nov. Int J Syst Evol Microbiol 2010; 60:1921–1937 [View Article][PubMed]
    [Google Scholar]
  26. Ferreira T, van Reenen C, Pagès S, Tailliez P, Malan AP et al. Photorhabdus luminescens subsp. noenieputensis subsp. nov., a symbiotic bacterium associated with a novel Heterorhabditis species related to Heterorhabditis indica. Int J Syst Evol Microbiol 2013; 63:1853–1858 [View Article][PubMed]
    [Google Scholar]
  27. Orozco RA, Hill T, Stock SP. Characterization and phylogenetic relationships of Photorhabdus luminescens subsp. sonorensis (γ-Proteobacteria: Enterobacteriaceae), the bacterial symbiont of the entomopathogenic nematode Heterorhabditis sonorensis (Nematoda: Heterorhabditidae). Curr Microbiol 2013; 66:30–39 [View Article][PubMed]
    [Google Scholar]
  28. Glaeser SP, Tobias NJ, Thanwisai A, Chantratita N, Bode HB et al. Photorhabdus luminescens subsp. namnaonensis subsp. nov., isolated from Heterorhabditis baujardi nematodes. Int J Syst Evol Microbiol 2017; 67:1046–1051 [View Article][PubMed]
    [Google Scholar]
  29. Grimont PAD, Steigerwalt AG, Boemare N, Hickman-Brenner FW, Deval C et al. Deoxyribonucleic acid relatedness and phenotypic study of the genus Xenorhabdus. Int J Syst Evol Microbiol 1984; 34:378–388 [View Article]
    [Google Scholar]
  30. Ezaki T, Hashimoto Y, Yabuuchi E. Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Evol Microbiol 1989; 39:224–229 [View Article]
    [Google Scholar]
  31. Farmer JJ, Jorgensen JH, Grimont PA, Akhurst RJ, Poinar GO et al. Xenorhabdus luminescens (DNA hybridization group 5) from human clinical specimens. J Clin Microbiol 1989; 27:1594–1600[PubMed]
    [Google Scholar]
  32. Rainey FA, Ehlers RU, Stackebrandt E. Inability of the polyphasic approach to systematics to determine the relatedness of the genera Xenorhabdus and Photorhabdus. Int J Syst Evol Microbiol 1995; 45:379–381 [View Article][PubMed]
    [Google Scholar]
  33. Akhurst RJ, Mourant RG, Baud L, Boemare NE. Phenotypic and DNA relatedness between nematode symbionts and clinical strains of the genus Photorhabdus (Enterobacteriaceae). Int J Syst Evol Microbiol 1996; 46:1034–1041 [View Article]
    [Google Scholar]
  34. Brunel B, Givaudan A, Lanois A, Akhurst RJ, Boemare N. Fast and accurate identification of Xenorhabdus and Photorhabdus species by restriction analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 1997; 63:574–580[PubMed]
    [Google Scholar]
  35. Liu J, Berry R, Poinar G, Moldenke A. Phylogeny of Photorhabdus and Xenorhabdus species and strains as determined by comparison of partial 16S rRNA gene sequences. Int J Syst Evol Microbiol 1997; 47:948–951 [View Article][PubMed]
    [Google Scholar]
  36. Vandamme P, Pot B, Gillis M, de Vos P, Kersters K et al. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 1996; 60:407–438[PubMed]
    [Google Scholar]
  37. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Systematic Microbiol 1987; 37:463–464 [View Article]
    [Google Scholar]
  38. Ferreira T, van Reenen CA, Endo A, Tailliez P, Pagès S et al. Photorhabdus heterorhabditis sp. nov., a symbiont of the entomopathogenic nematode Heterorhabditis zealandica. Int J Syst Evol Microbiol 2014; 64:1540–1545 [View Article][PubMed]
    [Google Scholar]
  39. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 1998; 95:3140–3145 [View Article][PubMed]
    [Google Scholar]
  40. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PA, Kämpfer P et al. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 2002; 52:1043–1047 [View Article][PubMed]
    [Google Scholar]
  41. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T et al. Opinion: Re-evaluating prokaryotic species. Nat Rev Microbiol 2005; 3:733–739 [View Article][PubMed]
    [Google Scholar]
  42. Vanlaere E, Baldwin A, Gevers D, Henry D, de Brandt E et al. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 2009; 59:102–111 [View Article][PubMed]
    [Google Scholar]
  43. López-Hermoso C, de La Haba RR, Sánchez-Porro C, Papke RT, Ventosa A. Assessment of multiLocus sequence analysis as a valuable tool for the classification of the genus Salinivibrio. Front Microbiol 2017; 8:1107 [View Article][PubMed]
    [Google Scholar]
  44. Geldenhuys J, Malan AP, Dicks LM. First report of the isolation of the symbiotic bacterium Photorhabdus luminescens subsp. laumondii associated with Heterorhabditis safricana from South Africa. Curr Microbiol 2016; 73:790–795 [View Article][PubMed]
    [Google Scholar]
  45. Auch AF, Klenk HP, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article][PubMed]
    [Google Scholar]
  46. Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article][PubMed]
    [Google Scholar]
  47. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  48. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article][PubMed]
    [Google Scholar]
  49. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
    [Google Scholar]
  50. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article][PubMed]
    [Google Scholar]
  51. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 2014; 9:2 [View Article][PubMed]
    [Google Scholar]
  52. Rodrigo-Torres L, Pujalte MJ, Arahal DR. Draft genome of Leisingera aquaemixtae CECT 8399T, a member of the Roseobacter clade isolated from a junction of fresh and ocean water in Jeju Island, South Korea. Genomics data 2016; 7:233–236 [View Article][PubMed]
    [Google Scholar]
  53. Tortoli E, Kohl TA, Brown-Elliott BA, Trovato A, Leão SC et al. Emended description of Mycobacterium abscessus, Mycobacterium abscessus subsp. abscessus and Mycobacterium abscessus subsp. bolletii and designation of Mycobacterium abscessus subsp. massiliense comb. nov. Int J Syst Evol Microbiol 2016; 66:4471–4479 [View Article][PubMed]
    [Google Scholar]
  54. Bedding RA, Akhurst RJ. A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 1975; 21:109–110 [View Article]
    [Google Scholar]
  55. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  56. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  57. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol 2012; 13:R56 [View Article][PubMed]
    [Google Scholar]
  58. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article][PubMed]
    [Google Scholar]
  59. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article][PubMed]
    [Google Scholar]
  60. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
    [Google Scholar]
  61. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article][PubMed]
    [Google Scholar]
  62. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36:W465–W469 [View Article][PubMed]
    [Google Scholar]
  63. Dereeper A, Audic S, Claverie JM, Blanc G. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 2010; 10:8 [View Article][PubMed]
    [Google Scholar]
  64. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  65. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [View Article][PubMed]
    [Google Scholar]
  66. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003; 52:696–704 [View Article][PubMed]
    [Google Scholar]
  67. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 2006; 55:539–552 [View Article][PubMed]
    [Google Scholar]
  68. Chevenet F, Brun C, Bañuls AL, Jacq B, Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 2006; 7:439 [View Article][PubMed]
    [Google Scholar]
  69. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article][PubMed]
    [Google Scholar]
  70. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 2016; 41:95–98
    [Google Scholar]
  71. Kuhnert P, Bisgaard M, Korczak BM, Schwendener S, Christensen H et al. Identification of animal Pasteurellaceae by MALDI-TOF mass spectrometry. J Microbiol Methods 2012; 89:1–7 [View Article][PubMed]
    [Google Scholar]
  72. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586[PubMed]
    [Google Scholar]
  73. Kuykendall LD, Roy MA, O'Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Evol Microbiol 1988; 38:358–361 [View Article]
    [Google Scholar]
  74. Kämpfer P, Kroppenstedt RM. Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 1996; 42:989–1005 [View Article]
    [Google Scholar]
  75. Diogo A, Veríssimo A, Nobre MF, da Costa MS. Usefulness of fatty acid composition for differentiation of Legionella species. J Clin Microbiol 1999; 37:2248–2254[PubMed]
    [Google Scholar]
  76. Vrain TC, Wakarchuk DA, Levesque AC, Hamilton RI. Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundam Appl Nematol 15:563–573
    [Google Scholar]
  77. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article][PubMed]
    [Google Scholar]
  78. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  79. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article][PubMed]
    [Google Scholar]
  80. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  81. Parker CT, Tindall BJ, Garrity GM. International Code of Nomenclature of Prokaryotes (Prokaryotic Code, 2008 Revision). Int J Syst Evol Microbiol 2016 [View Article]
    [Google Scholar]
  82. Glaeser SP, Kämpfer P. Multilocus sequence analysis (MLSA) in prokaryotic taxonomy. Syst Appl Microbiol 2015; 38:237–245 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002820
Loading
/content/journal/ijsem/10.1099/ijsem.0.002820
Loading

Data & Media loading...

Supplements

Supplementary File 2

PDF
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