1887

Abstract

In recent years, the results of genome-based phylogenetic analyses have contributed to microbial systematics by increasing the availability of sequenced microbial genomes. Therefore, phylogenomic analysis within large taxa in the phylum has appeared as a useful tool to clarify the taxonomic positions of ambiguous groups. In this study, we provide a revision of the actinobacterial family using a large collection of genome data and phylogenomics approaches. The phylogenomic analyses included the publicly available genome data of the members of the family and the state-of-the-art tools are used to infer the taxonomic affiliation of these species within the family. By comparing genome-based and 16S rRNA gene-based trees, as well as pairwise genome comparisons, the recently described genera and are combined in the genus . In conclusion, a comprehensive phylogenomic revision of the family is proposed.

Funding
This study was supported by the:
  • Ondokuz Mayis Üniversitesi (Award PYO.FEN.1901.16.001)
    • Principle Award Recipient: Nevzat Sahin
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004073
2020-03-04
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/4/2569.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004073&mimeType=html&fmt=ahah

References

  1. 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; 9:1–119 [View Article]
    [Google Scholar]
  2. Goodfellow M, Quintana E. Family 1. Streptosporangiaceae Goodfellow, Stanton, Simpson and Minnikin 1990a 321VP. Bergey’s manual of systematic bacteriology 2012; 5:
    [Google Scholar]
  3. Zhi X-Y, Li W-J, 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]
  4. Goodfellow M, Stanton L, Simpson K, Minnikin D. Numerical and chemical classification of Actinoplanes and some related actinomycetes. Microbiology 1990; 136:19–36
    [Google Scholar]
  5. Ara I, Kudo T. Sphaerosporangium gen. nov., a new member of the family Streptosporangiaceae, with descriptions of three new species as Sphaerosporangium melleum sp. nov., Sphaerosporangium rubeum sp. nov. and Sphaerosporangium cinnabarinum sp. nov., and transfer of Streptosporangium viridialbum Nonomura and Ohara 1960 to Sphaerosporangium viridialbum comb. nov. Actinomycetologica 2007; 21:11–21 [View Article]
    [Google Scholar]
  6. Meyers PR. Gyrase subunit B amino acid signatures for the actinobacterial family Streptosporangiaceae . Syst Appl Microbiol 2014; 37:252–260 [View Article]
    [Google Scholar]
  7. Meyers PR. Analysis of recombinase A (recA/RecA) in the actinobacterial family Streptosporangiaceae and identification of molecular signatures. Syst Appl Microbiol 2015; 38:567–577 [View Article]
    [Google Scholar]
  8. Meyers PR. Molecular-signature analyses support the establishment of the actinobacterial genus Sphaerimonospora (Mingma et al. 2016). Syst Appl Microbiol 2017; 40:423–429 [View Article]
    [Google Scholar]
  9. Carro L, Nouioui I, Sangal V, Meier-Kolthoff JP, Trujillo ME et al. Genome-Based classification of micromonosporae with a focus on their biotechnological and ecological potential. Sci Rep 2018; 8:525 [View Article]
    [Google Scholar]
  10. Jensen PR. Review of microbial ecology. J Nat Prod 2017; 80:232
    [Google Scholar]
  11. MdC M-C, Meier-Kolthoff JP, Zhang D-F, Yaramis A, Rohde M et al. Genome-scale data call for a taxonomic rearrangement of Geodermatophilaceae . Front Microbiol 2017; 8:2501
    [Google Scholar]
  12. Sangal V, Goodfellow M, Jones AL, Schwalbe EC, Blom J et al. Next-Generation systematics: an innovative approach to resolve the structure of complex prokaryotic taxa. Sci Rep 2016; 6:38392 [View Article]
    [Google Scholar]
  13. Tang H, Shi X, Wang X, Hao H, Zhang X-M et al. Environmental controls over actinobacteria communities in ecological sensitive Yanshan Mountains zone. Front Microbiol 2016; 7:343 [View Article]
    [Google Scholar]
  14. Gupta RS, Lo B, Son J. Phylogenomics and comparative genomic studies robustly support division of the genus Mycobacterium into an emended genus Mycobacterium and four novel genera. Front Microbiol 2018; 9:67 [View Article]
    [Google Scholar]
  15. Lugli GA, Milani C, Turroni F, Duranti S, Mancabelli L et al. Comparative genomic and phylogenomic analyses of the Bifidobacteriaceae family. BMC Genomics 2017; 18:568 [View Article]
    [Google Scholar]
  16. Jiang Z, Xiao M, Yang L-L, Zhi X-Y, Li W-J. Genome-based taxonomic classification within the family Thermoactinomycetaceae . Int J Syst Evol Microbiol 2019; 69:2028–2036 [View Article]
    [Google Scholar]
  17. Hu D, Cha G, Gao B. A phylogenomic and molecular markers based analysis of the class acidimicrobiia. Front Microbiol 2018; 9:987 [View Article]
    [Google Scholar]
  18. Feng Y-Z, Yang L-L, Gao S, Ji Y, Yin M et al. Bailinhaonella thermotolerans gen. nov., sp. nov., a new member of the order Streptosporangiales . Int J Syst Evol Microbiol 2019; 69:1903–1909 [View Article]
    [Google Scholar]
  19. Li L, Gui Y-H, Xu Q-H, Lin H-W, Lu Y-H. Spongiactinospora rosea gen. nov., sp. nov., a new member of the family Streptosporangiaceae . Int J Syst Evol Microbiol 2019; 69:427–433 [View Article]
    [Google Scholar]
  20. Saygin H, Ay H, Guven K, Cetin D, Sahin N. Desertiactinospora gelatinilytica gen. nov., sp. nov., a new member of the family Streptosporangiaceae isolated from the Karakum Desert. Antonie van Leeuwenhoek 2019; 112:409–423 [View Article]
    [Google Scholar]
  21. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2019; 69:1247–1250 [View Article]
    [Google Scholar]
  22. Oren A, Garrity GM. Notification that new names of prokaryotes, new combinations, and new taxonomic opinions have appeared in volume 69, part 2 of the IJSEM. Int J Syst Evol Microbiol 2019; 69:1251–1252 [View Article]
    [Google Scholar]
  23. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article]
    [Google Scholar]
  24. Boratyn GM, Camacho C, Cooper PS, Coulouris G, Fong A et al. BLAST: a more efficient report with usability improvements. Nucleic Acids Res 2013; 41:W29–W33 [View Article]
    [Google Scholar]
  25. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002; 30:1575–1584 [View Article]
    [Google Scholar]
  26. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
    [Google Scholar]
  27. Eddy SR. Profile hidden Markov models. Bioinformatics 1998; 14:755–763 [View Article]
    [Google Scholar]
  28. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007; 56:564–577 [View Article]
    [Google Scholar]
  29. Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article]
    [Google Scholar]
  30. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
    [Google Scholar]
  31. Davis JJ, Gerdes S, Olsen GJ, Olson R, Pusch GD et al. PATtyFams: protein families for the microbial genomes in the PATRIC database. Front Microbiol 2016; 7:118 [View Article]
    [Google Scholar]
  32. Cock PJA, Antao T, Chang JT, Chapman BA, Cox CJ et al. Biopython: freely available python tools for computational molecular biology and bioinformatics. Bioinformatics 2009; 25:1422–1423 [View Article]
    [Google Scholar]
  33. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008; 57:758–771 [View Article]
    [Google Scholar]
  34. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article]
    [Google Scholar]
  35. Lagesen K, Hallin P, Rødland E, Stærfeldt H, Rognes T et al. RNammer: consistent annotation of rRNA genes in genomic sequences. Nucleic Acids Res 2007; 35:3100–3108
    [Google Scholar]
  36. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
    [Google Scholar]
  37. 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]
  38. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program: table 1. Mol Biol Evol 2015; 32:2798–2800 [View Article]
    [Google Scholar]
  39. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
  40. Ł K, Botzki A, Coppens F, Vandepoele K, Van Bel M. PhyD3: a phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics 2017; 33:2946–2947
    [Google Scholar]
  41. Liu Y, Lai Q, Göker M, Meier-Kolthoff JP, Wang M et al. Genomic insights into the taxonomic status of the Bacillus cereus group. Sci Rep 2015; 5:14082 [View Article]
    [Google Scholar]
  42. 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]
    [Google Scholar]
  43. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article]
    [Google Scholar]
  44. Goris J, Klappenbach JA, Vandamme P, Coenye T, Konstantinidis KT 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]
    [Google Scholar]
  45. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article]
    [Google Scholar]
  46. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article]
    [Google Scholar]
  47. Couch JN. A new genus and family of the Actinomycetales, with a revision of the genus Actinoplanes . J Elisha Mitchell Sci Soc 1955; 71:148–155
    [Google Scholar]
  48. Tamura T, Suzuki S, Hatano K. Acrocarpospora gen. nov., a new genus of the order Actinomycetales . Int J Syst Evol Microbiol 2000; 50:1163–1171 [View Article]
    [Google Scholar]
  49. Kudo T, Itoh T, Miyadoh S, Shomura T, Seino A. Herbidospora gen. nov., a new genus of the family Streptosporangiaceae Goodfellow et al. 1990. Int J Syst Bacteriol 1993; 43:319–328 [View Article]
    [Google Scholar]
  50. Nonomura H, Ohara Y. Distribution of actinomycetes in soil II. Microbispora, a new genus of Streptomycetaceae . J Ferment Technol 1957; 35:307–311
    [Google Scholar]
  51. Thiemann JE, Pagani H, Beretta G. A new genus of the Actinomycetales: Microtetraspora gen.nov. J Gen Microbiol 1968; 50:295–303 [View Article]
    [Google Scholar]
  52. Zhang Z, Wang Y, Ruan J. Reclassification of Thermomonospora and Microtetraspora . Int J Syst Bacteriol 1998; 48:411–422 [View Article]
    [Google Scholar]
  53. Thiemann JE, Beretta G. A new genus of the Actinoplanaceae: Planobispora, gen. nov. Archiv. Mikrobiol. 1968; 62:157–166 [View Article]
    [Google Scholar]
  54. Thiemann J, Pagani H, Beretta G. A new genus of the Actinoplanaceae: Planomonospora gen. nov. Giorn Microbiol 1967; 15:27–38
    [Google Scholar]
  55. Runmao H, Guizhen W, Junying L. A new genus of actinomycetes, Planotetraspora gen. nov. Int J Syst Bacteriol 1993; 43:468–470 [View Article]
    [Google Scholar]
  56. Zhang Y-Q, Liu H-Y, Yu L-Y, Lee J-C, Park D-J et al. Sinosporangium album gen. nov., sp. nov., a new member of the suborder Streptosporangineae . Int J Syst Evol Microbiol 2011; 61:592–597 [View Article]
    [Google Scholar]
  57. Mingma R, Duangmal K, Také A, Inahashi Y, O Mura S et al. Proposal of Sphaerimonospora cavernae gen. nov., sp. nov. and transfer of Microbispora mesophila (Zhang et al., 1998) to Sphaerimonospora mesophila comb. nov. and Microbispora thailandensis (Duangmal et al., 2012) to Sphaerimonospora thailandensis comb. nov. Int J Syst Evol Microbiol 2016; 66:1735–1744 [View Article]
    [Google Scholar]
  58. Zhou E-M, Tang S-K, Sjøholm C, Song Z-Q, Yu T-T et al. Thermoactinospora rubra gen. nov., sp. nov., a thermophilic actinomycete isolated from Tengchong, Yunnan Province, south-west China. Antonie Van Leeuwenhoek 2012; 102:177–185 [View Article]
    [Google Scholar]
  59. Wang Y, Zhang Z, Ruan J. A proposal to transfer Microbispora bispora (Lechevalier 1965) to a new genus, Thermobispora gen. nov., as Thermobispora bispora comb. nov. Int J Syst Bacteriol 1996; 46:933–938 [View Article]
    [Google Scholar]
  60. Zhou E-M, Yang L-L, Song Z-Q, Yu T-T, Nie G-X et al. Thermocatellispora tengchongensis gen. nov., sp. nov., a new member of the family Streptosporangiaceae . Int J Syst Evol Microbiol 2012; 62:2417–2423 [View Article]
    [Google Scholar]
  61. Goodfellow M, Maldonado LA, Quintana ET. Reclassification of Nonomuraea flexuosa (Meyer 1989) Zhang et al. 1998 as Thermopolyspora flexuosa gen. nov., comb. nov., nom. rev. Int J Syst Evol Microbiol 2005; 55:1979–1983 [View Article]
    [Google Scholar]
  62. Wu H, Liu B, Shao Y, Ou X, Huang F. Thermostaphylospora grisealba gen. nov., sp. nov., isolated from mushroom compost and transfer of Thermomonospora chromogena Zhang et al. 1998 to Thermostaphylospora chromogena comb. nov. Int J Syst Evol Microbiol 2018; 68:602–608 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004073
Loading
/content/journal/ijsem/10.1099/ijsem.0.004073
Loading

Data & Media loading...

Supplements

Supplementary material 1

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