1887

Abstract

The family is a large and diverse family within the phylum . The members of the family are known for their ability to produce medically important secondary metabolites, notably antibiotics. In this study, 19 type strains showing low 16S rRNA gene similarity (<97.3 %) to other members of the family were identified and their high genetic diversity was reflected in a phylogenomic analysis using conserved universal proteins. This analysis resulted in the identification of six distinct genus-level clades, with two separated from the genus and four separated from the genus . Compared with members of the genera and , average amino acid identity (AAI) analysis of the novel genera identified gave values within the range of 63.9–71.3 %, as has been previously observed for comparisons of related but distinct bacterial genera. The whole-genome phylogeny was reconstructed using PhyloPhlAn 3.0 based on an optimized subset of conserved universal proteins, the results of AAI and percentage of conserved proteins (POCP) analyses indicated that these phylogenetically distinct taxa may be assigned to six novel genera, namely gen. nov., gen. nov., gen. nov., gen. nov., gen. nov. and gen. nov.

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2022-10-21
2024-05-04
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References

  1. Madhaiyan M, Saravanan VS, See-Too WS, Volpiano CG, Sant’ Anna FH et al. Genomic and phylogenomic insights into the family Streptomycetaceae lead to the proposal of six novel genera. Figshare 2022 [View Article]
    [Google Scholar]
  2. Waksman SA, Henrici AT. The nomenclature and classification of the actinomycetes. J Bacteriol 1943; 46:337–341 [View Article]
    [Google Scholar]
  3. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:2007 [View Article]
    [Google Scholar]
  4. Stackebrandt E, Rainey FA, Ward-rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 1997; 47:479–491 [View Article]
    [Google Scholar]
  5. Zhi XY, Li WJ, Stackebrandt E. An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 2009; 59:589–608 [View Article]
    [Google Scholar]
  6. Salam N, Jiao J-Y, Zhang X-T, Li W-J. Update on the classification of higher ranks in the phylum Actinobacteria. Int J Syst Evol Microbiol 2020; 70:1331–1355 [View Article]
    [Google Scholar]
  7. Kämpfer P. Streptomycetaceae. In Whitman WB. eds Bergey’s Manual of Systematics of Archaea and Bacteria Wiley Online Library; 2015 pp 1–11 [View Article]
    [Google Scholar]
  8. Omura S, Takahashi Y, Iwai Y, Tanaka H. Kitasatosporia, a new genus of the order Actinomycetales. J Antibiot (Tokyo) 1982; 35:1013–1019 [View Article]
    [Google Scholar]
  9. Wellington EM, Stackebrandt E, Sanders D, Wolstrup J, Jorgensen NO. Taxonomic status of Kitasatosporia, and proposed unification with Streptomyces on the basis of phenotypic and 16S rRNA analysis and emendation of Streptomyces Waksman and Henrici 1943, 339AL. Int J Syst Bacteriol 1992; 42:156–160 [View Article]
    [Google Scholar]
  10. Zhang Z, Wang Y, Ruan J. A proposal to revive the genus Kitasatospora (Omura, Takahashi, Iwai, and Tanaka 1982). Int J Syst Bacteriol 1997; 47:1048–1054 [View Article]
    [Google Scholar]
  11. Kim SB, Lonsdale J, Seong C-N, Goodfellow M. Streptacidiphilus gen. nov., acidophilic actinomycetes with wall chemotype I and emendation of the family Streptomycetaceae (Waksman and Henrici (1943)AL) emend. Rainey et al. 1997. Antonie Van Leeuwenhoek 2003; 83:107–116 [View Article]
    [Google Scholar]
  12. Huang M-J, Rao MPN, Salam N, Xiao M, Huang H-Q et al. Allostreptomyces psammosilenae gen. nov., sp. nov., an endophytic actinobacterium isolated from the roots of Psammosilene tunicoides and emended description of the family Streptomycetaceae [Waksman and Henrici (1943)AL] emend. Rainey et al. 1997, emend. Kim et al. 2003, emend. Zhi et al. 2009. Int J Syst Evol Microbiol 2017; 67:288–293 [View Article]
    [Google Scholar]
  13. Li Y, Wang M, Sun Z-Z, Xie B-B. Comparative genomic insights into the taxonomic classification, diversity, and secondary metabolic potentials of Kitasatospora, a genus closely related to Streptomyces. Front Microbiol 2021; 12:683814 [View Article]
    [Google Scholar]
  14. Kämpfer P. The family Streptomycetaceae part 1: taxonomy. In Dworkin M. eds The Prokaryotes, Vol 3, Bacteria: Firmicutes, Actinomycetes New York: Springer; 2006 pp 538–604 [View Article]
    [Google Scholar]
  15. Glaeser SP, Kämpfer P. Streptomycetaceae: phylogeny, ecology and pathogenicity. In ELS Chichester: John Wiley & Sons, Ltd; 2016 pp 1–12 [View Article]
    [Google Scholar]
  16. Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B et al. Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek 2012; 101:73–104 [View Article]
    [Google Scholar]
  17. Labeda DP, Dunlap CA, Rong X, Huang Y, Doroghazi JR et al. Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis. Antonie Van Leeuwenhoek 2017; 110:563–583 [View Article]
    [Google Scholar]
  18. Komaki H, Tamura T. Reclassification of Streptomyces castelarensis and Streptomyces sporoclivatus as later heterotypic synonyms of Streptomyces antimycoticus. Int J Syst Evol Microbiol 2020; 70:1099–1105 [View Article]
    [Google Scholar]
  19. Madhaiyan M, Saravanan VS, See-Too WS. Genome-based analyses reveal the presence of 12 heterotypic synonyms in the genus Streptomyces and emended descriptions of Streptomyces bottropensis, Streptomyces celluloflavus, Streptomyces fulvissimus, Streptomyces glaucescens, Streptomyces murinus, and Streptomyces variegatus. Int J Syst Evol Microbiol 2020; 70:3924–3929 [View Article]
    [Google Scholar]
  20. Volpiano CG, Sant’Anna FH, da Mota FF, Sangal V, Sutcliffe I et al. Proposal of Carbonactinosporaceae fam. nov. within the class Actinomycetia. Reclassification of Streptomyces thermoautotrophicus as Carbonactinospora thermoautotrophica gen. nov., comb. nov. Syst Appl Microbiol 2021; 44:126223 [View Article]
    [Google Scholar]
  21. 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]
    [Google Scholar]
  22. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for Bacteria and Archaea based on a standard genome relatedness index. mBio 2020; 14:e02475
    [Google Scholar]
  23. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article]
    [Google Scholar]
  24. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article]
    [Google Scholar]
  25. Schliep KP. Phangorn: phylogenetic analysis in R. Bioinformatics 2011; 27:592–593 [View Article]
    [Google Scholar]
  26. Revell LJ. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 2012; 3:217–223 [View Article]
    [Google Scholar]
  27. Yu G, Smith DK, Zhu H, Guan Y, Lam TTY. GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017; 8:28–36
    [Google Scholar]
  28. Myers EW, Miller W. Optimal alignments in linear space. Bioinformatics 1988; 4:11–17 [View Article]
    [Google Scholar]
  29. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article]
    [Google Scholar]
  30. Asnicar F, Thomas AM, Beghini F, Mengoni C, Manara S et al. Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0. Nat Commun 2020; 11:2500 [View Article]
    [Google Scholar]
  31. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article]
    [Google Scholar]
  32. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
    [Google Scholar]
  33. Blom J, Kreis J, Spänig S, Juhre T, Bertelli C et al. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 2016; 44:W22–8 [View Article]
    [Google Scholar]
  34. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article]
    [Google Scholar]
  35. Guo Y, Zheng W, Rong X, Huang Y. A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 2008; 58:149–159 [View Article]
    [Google Scholar]
  36. Nouioui I, Klenk HP, Igual JM, Gulvik CA, Lasker BA et al. Streptacidiphilus bronchialis sp. nov., a ciprofloxacin-resistant bacterium from a human clinical specimen; reclassification of Streptomyces griseoplanus as Streptacidiphilus griseoplanus comb. nov. and emended description of the genus Streptacidiphilus. Int J Syst Evol Microbiol 2019; 69:1047–1056 [View Article]
    [Google Scholar]
  37. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014; 42:e73 [View Article]
    [Google Scholar]
  38. Nicholson AC, Gulvik CA, Whitney AM, Humrighouse BW, Bell ME et al. Division of the genus Chryseobacterium: Observation of discontinuities in amino acid identity values, a possible consequence of major extinction events, guides transfer of nine species to the genus Epilithonimonas, eleven species to the genus Kaistella, and three species to the genus Halpernia gen. nov., with description of Kaistella daneshvariae sp. nov. and Epilithonimonas vandammei sp. nov. derived from clinical specimens. Int J Syst Evol Microbiol 2020; 70:4432–4450 [View Article]
    [Google Scholar]
  39. Malik A, Kim YR, Kim SB. Genome mining of the genus Streptacidiphilus for biosynthetic and biodegradation potential. Genes 2020; 11:E1166 [View Article]
    [Google Scholar]
  40. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article]
    [Google Scholar]
  41. Wang L, Huang Y, Liu Z, Goodfellow M, Rodríguez C. Streptacidiphilus oryzae sp. nov., an actinomycete isolated from rice-field soil in Thailand. Int J Syst Evol Microbiol 2006; 56:1257–1261 [View Article]
    [Google Scholar]
  42. Noble M, Noble D, Fletton RA. G2201-C, A new cyclopentenedione antibiotic, isolated from the fermentation broth of Streptomyces cattleya. J Antibiot 1978; 31:15–18 [View Article]
    [Google Scholar]
  43. Kahan JS, Kahan FM, Goegelman R, Currie SA, Jackson M et al. Thienamycin, a new beta-lactam antibiotic. I. Discovery, taxonomy, isolation and physical properties. J Antibiot (Tokyo) 1979; 32:1–12 [View Article]
    [Google Scholar]
  44. Barbe V, Bouzon M, Mangenot S, Badet B, Poulain J et al. Complete genome sequence of Streptomyces cattleya NRRL 8057, a producer of antibiotics and fluorometabolites. J Bacteriol 2011; 193:5055–5056 [View Article]
    [Google Scholar]
  45. Zhao C, Li P, Deng Z, Ou H-Y, McGlinchey RP et al. Insights into fluorometabolite biosynthesis in Streptomyces cattleya DSM 46488 through genome sequence and knockout mutants. Bioorg Chem 2012; 44:1–7 [View Article]
    [Google Scholar]
  46. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the Roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018; 68:2393–2411 [View Article]
    [Google Scholar]
  47. Sangal V, Goodfellow M, Blom J, Tan GYA, Klenk HP et al. Revisiting the taxonomic status of the biomedically and industrially important genus Amycolatopsis, using a phylogenomic approach. Front Microbiol 2018; 9:2281 [View Article]
    [Google Scholar]
  48. Zhu WZ, Ge YM, Gao HM, Dai J, Zhang XL et al. Gephyromycinifex aptenodytis gen. nov., sp. nov., isolated from gut of antarctic emperor penguin Aptenodytes forsteri. Antonie Van Leeuwenhoek 2021; 114:2003–2017 [View Article]
    [Google Scholar]
  49. Hsiao NH, Kirby R. Comparative genomics of Streptomyces avermitilis, Streptomyces cattleya, Streptomyces maritimus and Kitasatospora aureofaciens using a Streptomyces coelicolor microarray system. Antonie Van Leeuwenhoek 2008; 93:1–25 [View Article]
    [Google Scholar]
  50. Saintpierre-Bonaccio D, Amir H, Pineau R, Lemriss S, Goodfellow M. Streptomyces ferralitis sp. nov., a novel streptomycete isolated from a New-Caledonian ultramafic soil. Int J Syst Evol Microbiol 2004; 54:2061–2065 [View Article]
    [Google Scholar]
  51. Guo X, Zhang L, Li X, Gao Y, Ruan J et al. Streptomyces rubrisoli sp. nov., neutrotolerant acidophilic actinomycetes isolated from red soil. Int J Syst Evol Microbiol 2015; 65:3103–3108 [View Article]
    [Google Scholar]
  52. Chantavorakit T, Klaysubun C, Duangmal K. Streptomyces acididurans sp. nov., isolated from peat swamp forest soil. Int J Syst Evol Microbiol 2021; 71:4849 [View Article]
    [Google Scholar]
  53. Duangupama T, Intaraudom C, Pittayakhajonwut P, Tadtong S, Thawai C. Streptomyces epipremni sp. nov., an endophytic actinomycete isolated from the root of Epipremnum aureum. Int J Syst Evol Microbiol 2022; 72:005179 [View Article]
    [Google Scholar]
  54. Ser H-L, Zainal N, Palanisamy UD, Goh B-H, Yin W-F et al. Streptomyces gilvigriseus sp. nov., a novel actinobacterium isolated from mangrove forest soil. Antonie Van Leeuwenhoek 2015; 107:1369–1378 [View Article]
    [Google Scholar]
  55. Shomura T, Amano S, Yoshida J, Ezaki N, Ito T et al. Actinosporangium vitaminophilum sp. nov. Int J Syst Bacteriol 1983; 33:557–564 [View Article]
    [Google Scholar]
  56. Goodfellow M, Williams ST, Alderson G. Transfer of Actinosporangium violaceum Krasil’nikov and Yuan, Actinosporangium vitaminophilum Shomura et al. and Actinopycnidium caeruleum Krasil’nikov to the genus Streptomyces, with amended descriptions of the species. Syst Appl Microbiol 1986; 8:61–64 [View Article]
    [Google Scholar]
  57. Zhao J, Guo L, Liu C, Bai L, Han C et al. Streptomyces tyrosinilyticus sp. nov., a novel actinomycete isolated from river sediment. Int J Syst Evol Microbiol 2015; 65:3091–3096 [View Article]
    [Google Scholar]
  58. Krassilnikov NA, Yuan CS. Actinosporangium, a new genus of the family actinoplanaceae. Izvestiya akademii nauk SSSR seriya biologicheskaya 1963; 8:113–116
    [Google Scholar]
  59. Wang H-F, Li Q-L, Xiao M, Zhang Y-G, Zhou X-K et al. Streptomyces capparidis sp. nov., a novel endophytic actinobacterium isolated from fruits of Capparis spinosa L. Int J Syst Evol Microbiol 2017; 67:133–137 [View Article]
    [Google Scholar]
  60. Liu N, Wang H, Liu M, Gu Q, Zheng W et al. Streptomyces alni sp. nov., a daidzein-producing endophyte isolated from a root of Alnus nepalensis D. Don. Int J Syst Evol Microbiol 2009; 59:254–258 [View Article]
    [Google Scholar]
  61. Li C, Jin P, Liu C, Ma Z, Zhao J et al. Streptomyces bryophytorum sp. nov., an endophytic actinomycete isolated from moss (Bryophyta). Antonie Van Leeuwenhoek 2016; 109:1209–1215 [View Article]
    [Google Scholar]
  62. Huang Y, Li W, Wang L, Lanoot B, Vancanneyt M et al. Streptomyces glauciniger sp. nov., a novel mesophilic streptomycete isolated from soil in south China. Int J Syst Evol Microbiol 2004; 54:2085–2089 [View Article]
    [Google Scholar]
  63. Xu C, Wang L, Cui Q, Huang Y, Liu Z et al. Neutrotolerant acidophilic Streptomyces species isolated from acidic soils in China: Streptomyces guanduensis sp. nov., Streptomyces paucisporeus sp. nov., Streptomyces rubidus sp. nov. and Streptomyces yanglinensis sp. nov. Int J Syst Evol Microbiol 2006; 56:1109–1115 [View Article]
    [Google Scholar]
  64. Li C, Cao P, Jiang M, Sun T, Shen Y et al. Streptomyces oryziradicis sp. nov., a novel actinomycete isolated from rhizosphere soil of rice (Oryza sativa L.). Int J Syst Evol Microbiol 2020; 70:465–472 [View Article]
    [Google Scholar]
  65. Xing J, Jiang X, Kong D, Zhou Y, Li M et al. Streptomyces soli sp. nov., isolated from birch forest soil. Arch Microbiol 2020; 202:1687–1692 [View Article]
    [Google Scholar]
  66. Kim SB, Seong CN, Jeon SJ, Bae KS, Goodfellow M. Taxonomic study of neutrotolerant acidophilic actinomycetes isolated from soil and description of Streptomyces yeochonensis sp. nov. Int J Syst Evol Microbiol 2004; 54:211–214 [View Article]
    [Google Scholar]
  67. Backus EJ, Tresner HD, Campbell TH. The nucleocidin and alazopetin producing organisms: two new species of Streptomyces. Antibiot Chemother 1957; 7:532–541
    [Google Scholar]
  68. Kämpfer P. Genus incertae sedis II. Streptacidiphilus Kim, Lonsdale, Seong and Goodfellow 2003a, 1219VP (Effective publication: Kim, Lonsdale, Seong and Goodfellow 2003b, 115.). In Bergey’s Manual of Systematic Bacteriology, 2nd ed. vol 5 New York: Springer; 2012 pp 1777–1805
    [Google Scholar]
  69. Kim SB, Lonsdale J, Seong CN, Goodfellow G. Streptacidiphilus gen. nov., acidophilic actinomycetes with wall chemotype I and emendation of the family Streptomycetaceae (Waksman and Henrici (1943) AL) emend. Rainey et al. 1997. Antonie Van Leeuwenhoek 1997; 83:107–116
    [Google Scholar]
  70. Shirling EB, Gottlieb D. Retrospective evaluation of International Streptomyces Project taxonomic criteria. In In Actinomycetes: The Boundary Microorganisms Baltimore: University Park Press; 1977 pp 9–41
    [Google Scholar]
  71. Ōmura S, Takahashi Y, Iwai Y. Genus Kitasatosporia. In Williams, Sharpe and Holt (Ed) Bergey’s Manual of Systematic Bacteriology vol 4 Baltimore: Williams & Wilkins; 1989 pp 2594–2598
    [Google Scholar]
  72. Lonsdale JT. Aspects of the biology of acidophilic actinomycetes. PhD Thesis UK: University of Newcastle; 1985
    [Google Scholar]
  73. Williams ST, Goodfellow M, Alderson G. Genus Streptomyces Waksman and Henrici. In Williams, Sharpe and Holt (Ed) Bergey’s Manual of Systematic Bacteriology vol 4 Baltimore: Williams & Wilkins; 1989 pp 2452–2492
    [Google Scholar]
  74. Nakagaito Y, Shimazu A, Yokota A, Hasegawa T. Proposal of Streptomyces atroaurantiacus sp. nov. and Streptomyces kifunensis sp. nov. and transferring Kitasatosporia cystarginea Kusakabe and isono to the genus Streptomyces as Streptomyces cystargineus comb. nov. J Gen Appl Microbiol 1992; 38:627–633 [View Article]
    [Google Scholar]
  75. Antony-Babu S, Goodfellow M. Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune sand system. Antonie Van Leeuwenhoek 2008; 94:581–591 [View Article]
    [Google Scholar]
  76. Komaki H, Sakurai K, Hosoyama A, Kimura A, Trujilo ME et al. Diversity of PKS and NRPS gene clusters between Streptomyces abyssomicinicus sp. nov. and its taxonomic neighbor. J Antibiot 2020; 73:141–151 [View Article]
    [Google Scholar]
  77. Komaki H, Tamura T. Reclassification of Streptomyces rimosus subsp. paromomycinus as Streptomyces paromomycinus sp. nov. Int J Syst Evol Microbiol 2019; 69:2577–2583 [View Article]
    [Google Scholar]
  78. Roh SG, Kim M-K, Park S, Yun B-R, Park J et al. Streptacidiphilus pinicola sp. nov., isolated from pine grove soil. Int J Syst Evol Microbiol 2018; 68:3149–3155 [View Article]
    [Google Scholar]
  79. Ping X, Takahashi Y, Seino A, Iwai Y, Satoshi Ōmura S. Streptomyces scabrisporus sp. nov. Int J Syst Evol Microbiol 2004; 54:577–581 [View Article]
    [Google Scholar]
  80. Nagai A, Khan SH, Tamura T, Takagi M, Shin-Ya K. Streptomyces aomiensis sp. nov., isolated from a soil sample using the membrane-filter method. Int J Syst Evol Microbiol 2011; 61:947–950 [View Article]
    [Google Scholar]
  81. Mikami Y, Miyashita K, Arai T. Diaminopimelic acid profiles of alkalophilic and alkaline-resistant strains of Actinomycetes. J Gen Microbiol 1982; 128:1709–1712 [View Article]
    [Google Scholar]
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