1887

Abstract

The family Thermoactinomycetaceae comprises 43 validly published species, which were identified by a polyphasic taxonomic study based on molecular phylogenetics, physiological and biochemical characteristics. However, phylogenetic analysis merely based on 16S rRNA gene sequences cannot infer a robust and reliable phylogeny. For disentangling the phylogenetic relationships among members of this family, we used a large collection of genome data and the approach of phylogenomics, to re-examine their taxonomy. The topologies of phylogenomic trees are different from those of the 16S rRNA gene sequences. In addition, based on the average nucleotide identity, digital DNA–DNA hybridization, phenotypic and biochemical characteristics, we found that Laceyella sediminis should be reclassified as a later heterotypic synonym of Laceyella tengchongensis ; and reclassified Thermoactinomyces guangxiensis as Paenactinomyces guangxiensis gen. nov., comb. nov.; and establish Novibacillaceae fam. nov. to accommodate the genus Novibacillus as the type genus. In addition, compared to values calculated directly from genome sequences, the genomic DNA G+C contents mentioned in some species descriptions are too imprecise; and the corrected G+C content values have a significantly better fit to the phylogeny. Thus, the corresponding emendations of species descriptions are also proposed. In this paper, phylogenomics has been used to resolve the classification of the family Thermoactinomycetaceae .

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2019-05-08
2024-10-12
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References

  1. Yu TT, Zhang BH, Yao JC, Tang SK, Zhou EM et al. Lihuaxuella thermophila gen. nov., sp. nov., isolated from a geothermal soil sample in Tengchong, Yunnan, south-west China. Antonie van Leeuwenhoek 2012; 102:711–718 [View Article][PubMed]
    [Google Scholar]
  2. McVittie A, Wildermuth H, Hopwood DA. Fine structure and surface topography of endospores of thermoactinomyces vulgaris . J Gen Microbiol 1972; 71:367–381 [View Article]
    [Google Scholar]
  3. Li W, Xu P, Xu L, Jiang C. Actinomycetes resources in the environment. Microbiology China 2003; 30:125–127
    [Google Scholar]
  4. Tsiklinsky P. On the thermophilic moulds (in French). Ann Inst Pasteur 1899; 13:500–505
    [Google Scholar]
  5. Vos PD, Garrity GM, Jones D, Krieg NR, Ludwig W et al. Bergey's Manual of Systematic Bacteriology, 2nd ed. vol. 3 New York: Springer-Verlag; 2009 pp. 434–449
    [Google Scholar]
  6. Yassin AF, Hupfer H, Klenk HP, Siering C. Desmospora activa gen. nov., sp. nov., a thermoactinomycete isolated from sputum of a patient with suspected pulmonary tuberculosis and emended description of the family Thermoactinomycetaceae Matsuo et al. 2006. Int J Syst Evol Microbiol 2009; 59:454–459 [View Article][PubMed]
    [Google Scholar]
  7. Zhou EM, Yu TT, Liu L, Ming H, Yin YR et al. Geothermomicrobium terrae gen. nov., sp. nov., a novel member of the family Thermoactinomycetaceae . Int J Syst Evol Microbiol 2014; 64:2998–3004 [View Article][PubMed]
    [Google Scholar]
  8. von Jan M, Riegger N, Pötter G, Schumann P, Verbarg S et al. Kroppenstedtia eburnea gen. nov., sp. nov., a thermoactinomycete isolated by environmental screening and emended description of the family Thermoactinomycetaceae Matsuo et al. 2006 emend. Yassin et al. 2009. Int J Syst Evol Microbiol 2011; 61:2304–2310 [View Article][PubMed]
    [Google Scholar]
  9. Yoon JH, Kim IG, Shin YK, Park YH. Proposal of the genus Thermoactinomyces sensu stricto and three new genera, Laceyella, Thermoflavimicrobium and Seinonella, on the basis of phenotypic, phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 2005; 55:395–400 [View Article][PubMed]
    [Google Scholar]
  10. Li J, Zhang GT, Yang J, Tian XP, Wang FZ et al. Marininema mesophilum gen. nov., sp. nov., a thermoactinomycete isolated from deep sea sediment, and emended description of the family Thermoactinomycetaceae . Int J Syst Evol Microbiol 2012; 62:1383–1388 [View Article][PubMed]
    [Google Scholar]
  11. Matsuo Y, Katsuta A, Matsuda S, Shizuri Y, Yokota A et al. Mechercharimyces mesophilus gen. nov., sp. nov. and Mechercharimyces asporophorigenens sp. nov., antitumour substance-producing marine bacteria, and description of Thermoactinomycetaceae fam. nov. Int J Syst Evol Microbiol 2006; 56:2837–2842 [View Article]
    [Google Scholar]
  12. Addou AN, Schumann P, Spröer C, Hacene H, Cayol JL et al. Melghirimyces algeriensis gen. nov., sp. nov., a member of the family Thermoactinomycetaceae, isolated from a salt lake. Int J Syst Evol Microbiol 2012; 62:1491–1498 [View Article][PubMed]
    [Google Scholar]
  13. Yang G, Chen J, Zhou S. Novibacillus thermophilus gen. nov., sp. nov., a Gram-staining-negative and moderately thermophilic member of the family Thermoactinomycetaceae . Int J Syst Evol Microbiol 2015; 65:2591–2597 [View Article][PubMed]
    [Google Scholar]
  14. Hatayama K, Shoun H, Ueda Y, Nakamura A. Planifilum fimeticola gen. nov., sp. nov. and Planifilum fulgidum sp. nov., novel members of the family Thermoactinomycetaceae isolated from compost. Int J Syst Evol Microbiol 2005; 55:2101–2104 [View Article][PubMed]
    [Google Scholar]
  15. Tsubouchi T, Shimane Y, Mori K, Usui K, Hiraki T et al. Polycladomyces abyssicola gen. nov., sp. nov., a thermophilic filamentous bacterium isolated from hemipelagic sediment. Int J Syst Evol Microbiol 2013; 63:1972–1981 [View Article][PubMed]
    [Google Scholar]
  16. Kim M, Kim T, Ri S, Jiang F, Chang X et al. Risungbinella pyongyangensis gen. nov., sp. nov., a mesophilic member of the family Thermoactinomycetaceae isolated from an agricultural soil sample. Int J Syst Evol Microbiol 2015; 65:2726–2733 [View Article][PubMed]
    [Google Scholar]
  17. Park DJ, Dastager SG, Lee JC, Yeo SH, Yoon JH et al. Shimazuella kribbensis gen. nov., sp. nov., a mesophilic representative of the family Thermoactinomycetaceae . Int J Syst Evol Microbiol 2007; 57:2660–2664 [View Article][PubMed]
    [Google Scholar]
  18. Zhang Y, Li J, Tian X, Zhang S. Marinithermofilum abyssi gen. nov., sp. nov. and Desmospora profundinema sp. nov., isolated from a deep-sea sediment, and emended description of the genus Desmospora Yassin et al. 2009. Int J Syst Evol Microbiol 2015; 65:2622–2629 [View Article][PubMed]
    [Google Scholar]
  19. Buss SN, Cole JA, Hannett GE, Nazarian EJ, Nazarian L et al. Hazenella coriacea gen. nov., sp. nov., isolated from clinical specimens. Int J Syst Evol Microbiol 2013; 63:4087–4093 [View Article][PubMed]
    [Google Scholar]
  20. Frikha-Dammak D, Fardeau ML, Cayol JL, Ben Fguira-Fourati L, Najeh S et al. Paludifilum halophilum gen. nov., sp. nov., a thermoactinomycete isolated from superficial sediment of a solar saltern. Int J Syst Evol Microbiol 2016; 66:5371–5378 [View Article][PubMed]
    [Google Scholar]
  21. Guan X, Liu C, Fang B, Zhao J, Jin P et al. Baia soyae gen. nov., sp. nov., a mesophilic representative of the family Thermoactinomycetaceae, isolated from soybean root [Glycine max (L.) Merr]. Int J Syst Evol Microbiol 2015; 65:3754–3760 [View Article][PubMed]
    [Google Scholar]
  22. Hatayama K, Kuno T. Croceifilum oryzae gen. nov., sp. nov., isolated from rice paddy soil. Int J Syst Evol Microbiol 2015; 65:4061–4065 [View Article][PubMed]
    [Google Scholar]
  23. Li R, Zhu H, Ruan J, Qian W, Fang X et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010; 20:265–272 [View Article][PubMed]
    [Google Scholar]
  24. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article][PubMed]
    [Google Scholar]
  25. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article][PubMed]
    [Google Scholar]
  26. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 2014; 42:D560–D567 [View Article][PubMed]
    [Google Scholar]
  27. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article][PubMed]
    [Google Scholar]
  28. Delsuc F, Brinkmann H, Philippe H. Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 2005; 6:361–375 [View Article][PubMed]
    [Google Scholar]
  29. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  30. 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]
  31. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article][PubMed]
    [Google Scholar]
  32. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol 2008; 25:1307–1320 [View Article][PubMed]
    [Google Scholar]
  33. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  34. Librado P, Vieira FG, Sánchez-Gracia A, Kolokotronis SO, Rozas J. Mycobacterial phylogenomics: an enhanced method for gene turnover analysis reveals uneven levels of gene gain and loss among species and gene families. Genome Biol Evol 2014; 6:1454–1465 [View Article][PubMed]
    [Google Scholar]
  35. Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 1997; 14:685–695 [View Article][PubMed]
    [Google Scholar]
  36. Sukumaran J, Holder MT. DendroPy: a Python library for phylogenetic computing. Bioinformatics 2010; 26:1569–1571 [View Article][PubMed]
    [Google Scholar]
  37. 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]
  38. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 2011; 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  39. 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]
  40. Zhi XY, Jiang Z, Yang LL, Huang Y. The underlying mechanisms of genetic innovation and speciation in the family Corynebacteriaceae: a phylogenomics approach. Mol Phylogenet Evol 2017; 107:246–255 [View Article][PubMed]
    [Google Scholar]
  41. Lapierre P, Gogarten JP. Estimating the size of the bacterial pan-genome. Trends Genet 2009; 25:107–110 [View Article][PubMed]
    [Google Scholar]
  42. 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]
  43. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article][PubMed]
    [Google Scholar]
  44. Parker CT, Tindall BJ, Garrity GM. International code of nomenclature of prokaryotes. Int J Syst Evol Microbiol 2015
    [Google Scholar]
  45. Wu H, Liu B, Pan S. Thermoactinomyces guangxiensis sp. nov., a thermophilic actinomycete isolated from mushroom compost. Int J Syst Evol Microbiol 2015; 65:2859–2864 [View Article][PubMed]
    [Google Scholar]
  46. Zhang J, Tang SK, Zhang YQ, Yu LY, Klenk HP et al. Laceyella tengchongensis sp. nov., a thermophile isolated from soil of a volcano. Int J Syst Evol Microbiol 2010; 60:2226–2230 [View Article][PubMed]
    [Google Scholar]
  47. Ming H, Ji WL, Li S, Zhao ZL, Zhang LY et al. Laceyella thermophila sp. nov., a thermophilic bacterium isolated from a hot spring. Int J Syst Evol Microbiol 2017; 67:2953–2958 [View Article][PubMed]
    [Google Scholar]
  48. Lacey J, Cross T, Tsiklinsky GT. Genus Thermoactinomyces Tsiklinsky 1899, 501AL . In Williams ST, Shape ME, Holt JG. (editors) Bergey’s Manual of Systematic Bacteriology Baltimore: Williams & Wilkines; 1899 pp. 2574–2585
    [Google Scholar]
  49. Lacey J. Thermoactinomyces sacchari sp. nov., a thermophilic actinomycete causing bagassosis. J Gen Microbiol 1971; 66:327–338 [View Article][PubMed]
    [Google Scholar]
  50. Yang G, Qin D, Wu C, Yuan Y, Zhou S et al. Kroppenstedtia guangzhouensis sp. nov., a thermoactinomycete isolated from soil. Int J Syst Evol Microbiol 2013; 63:4077–4080 [View Article][PubMed]
    [Google Scholar]
  51. Han SI, Lee JC, Lee HJ, Whang KS. Planifilum composti sp. nov., a thermophile isolated from compost. Int J Syst Evol Microbiol 2013; 63:4557–4561 [View Article][PubMed]
    [Google Scholar]
  52. Zhang YX, Dong C, Biao S. Planifilum yunnanense sp. nov., a thermophilic thermoactinomycete isolated from a hot spring. Int J Syst Evol Microbiol 2007; 57:1851–1854 [View Article][PubMed]
    [Google Scholar]
  53. Yu Z, Wu C, Yang GQ, Zhou SG. Planifilum caeni sp. nov., a novel member of thermoactinomycete isolated from sludge compost. Curr Microbiol 2015; 70:135–140 [View Article][PubMed]
    [Google Scholar]
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