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Abstract

Two Gram-stain-positive, aerobic, non-spore-forming, non-motile, irregular rod-shaped actinobacteria, designated as D2-41 and D3-21, were isolated from soil samples collected in a natural cave in Jeju, Republic of Korea. Both of the isolates were shown to share 100 % 16S rRNA sequence identity. The cell wall contained -diaminopimelic acid, arabinose and galactose. The predominant menaquinone was MK-8(H). The polar lipids contained phosphatidylethanolamine, phosphatidylglycerol, phosphatidylinositol, phosphatidylinositol mannoside, an unidentified aminolipid, an unidentified aminoglycolipid, an unidentified phospholipid and two unidentified lipids. The predominant fatty acids were C and summed feature 3 (C 7 and/or iso-C 2-OH). Mycolic acids of C–C were present. The 16S rRNA gene trees showed that the organisms occupied a distinct position remotely located from recognized genera within the order , albeit with the 16S rRNA gene similarities of 97.0–97.1 % with , and . The genome sizes and DNA G+C contents of strains D2-41 and D3-21 were 4.77–4.88 Mbp and 69.8 mol%, respectively. Both of the isolates shared an average nucleotide identity of 99.4 % and digital DNA–DNA hybridization of 95.2 % to each other, revealing that strains D2-41 and D3-21 belonged to the same species. In the core genome-based phylogenomic tree, both of the isolates were found to be closely associated with members of the genus . However, strains D2-41 and D3-21 revealed the highest amino acid identity values (mean 66.5 %, range 66.2–67.0 % with the genus of the family , followed by the genus (mean 64.1 %, range 63.6–64.7 %) of the family . Based on the combined data obtained here, the novel isolates belong to a new genus of the new family for which the name gen. nov. sp. nov. is proposed, with aceae fam. nov. The type strain is strain D2-41 (=KACC 17930=DSM 101875).

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2024-02-12
2024-05-20
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References

  1. Goodfellow M, Jones AL. Order Corynebacteriales ord. nov. In Goodfellow M, Kämpfer P, Hussse H-J, Trujilo M, Suzuki K-I et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 235–243
    [Google Scholar]
  2. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2015; 65:3763–3767 [View Article] [PubMed]
    [Google Scholar]
  3. 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]
  4. 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] [PubMed]
    [Google Scholar]
  5. Gupta RS. Commentary: genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2019; 10:206 [View Article] [PubMed]
    [Google Scholar]
  6. Oren A, Garrity GM. List of changes in taxonomic opinion no.30. Notification of changes in taxonomic opinion previously published outside the IJSEM. Int J Syst Evol Microbiol 2019; 69:1850–1851 [View Article]
    [Google Scholar]
  7. 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] [PubMed]
    [Google Scholar]
  8. Katayama T, Kato T, Tanaka M, Douglas TA, Brouchkov A et al. Tomitella biformata gen. nov., sp. nov., a new member of the suborder Corynebacterineae isolated from a permafrost ice wedge. Int J Syst Evol Microbiol 2010; 60:2803–2807 [View Article] [PubMed]
    [Google Scholar]
  9. Lee SD, Kim IS, Verbarg S, Joung Y. Antrihabitans stalactiti gen nov. sp. nov., a new member of the family Nocardiaceae isolated from a cave. Int J Syst Evol Microbiol 2020; 70:5503–5511 [View Article] [PubMed]
    [Google Scholar]
  10. Sangal V, Goodfellow M, Jones AL, Sutcliffe IC. A stable home for an equine pathogen: valid publication of the binomial Prescottella equi gen. nov., comb. nov., and reclassification of four rhodococcal species into the genus Prescottella. Int J Syst Evol Microbiol 2022; 72:5551 [View Article] [PubMed]
    [Google Scholar]
  11. Kim S-M, Lee SD, Koh YS, Kim IS. Antrihabitans stalagmiti sp. nov., isolated from a larva cave and a proposal to transfer Rhodococcus cavernicola Lee et al. 2020 to a new genus Spelaeibacter as Spelaeibacter cavernicola gen. nov. comb. nov. Antonie van Leeuwenhoek 2022; 115:521–532 [View Article] [PubMed]
    [Google Scholar]
  12. Lee SD. Spelaeicoccus albus gen. nov., sp. nov., an actinobacterium isolated from a natural cave. Int J Syst Evol Microbiol 2013; 63:3958–3963 [View Article] [PubMed]
    [Google Scholar]
  13. Lee SD, Schumann P. Specibacter cremeus gen. nov., sp. nov., a new member of the family Micrococcaceae isolated from a natural cave. Int J Syst Evol Microbiol 2019; 69:1767–1774 [View Article]
    [Google Scholar]
  14. Lee SD, Kim IS. Rhodococcus spelaei sp. nov., isolated from a cave, and proposals that Rhodococcus biphenylivorans is a later synonym of Rhodococcus pyridinivorans, Rhodococcus qingshengii and Rhodococcus baikonurensis are later synonyms of Rhodococcus erythropolis, and Rhodococcus percolatus and Rhodococcus imtechensis are later synonyms of Rhodococcus opacus. Int J Syst Evol Microbiol 2021; 71:4890
    [Google Scholar]
  15. Lee SD, Kim IS, Schumann P, Song G. Leekyejoonella antrihumi gen. nov., sp. nov., a new member of the family Dermacoccaceae isolated from a cave soil. Int J Syst Evol Microbiol 2020; 70:3340–3347 [View Article] [PubMed]
    [Google Scholar]
  16. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  17. Hopwood DA, Bibb MJ, Chater KF, Kieser T, Bruton CJ et al. Genetic Manipulation of Streptomyces. A Laboratory Manual Norwich: John Innes Foundation; 1985
    [Google Scholar]
  18. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25:4876–4882 [View Article] [PubMed]
    [Google Scholar]
  19. 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]
  20. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 1971; 20:406 [View Article]
    [Google Scholar]
  21. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  22. Jukes TH, Cantor CR. Evolution of protein molecules. In Munro HN. eds Mammalian Protein Metabolism New York: Academic Press; 1969 pp 21–132
    [Google Scholar]
  23. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  24. Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article] [PubMed]
    [Google Scholar]
  25. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  26. Kim SM, Lee SD, Koh YS, Kim IS. Antrihabitans stalagmiti sp. nov., isolated from a larva cave and a proposal to transfer Rhodococcus cavernicola Lee et al. 2020 to a new genus Spelaeibacter as Spelaeibacter cavernicola gen. nov. comb. nov. Antonie van Leeuwenhoek 2022; 115:521–532 [View Article] [PubMed]
    [Google Scholar]
  27. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  28. 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] [PubMed]
    [Google Scholar]
  29. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
    [Google Scholar]
  30. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article] [PubMed]
    [Google Scholar]
  31. Terlouw BR, Blin K, Navarro-Muñoz JC, Avalon NE, Chevrette MG et al. MIBiG 3.0: a community-driven effort to annotate experimentally validated biosynthetic gene clusters. Nucleic Acids Res 2023; 51:D603–D610 [View Article] [PubMed]
    [Google Scholar]
  32. MacFaddin JF. Biochemical Tests for Identification of Medical Bacteria, 2nd. edn Baltimore: Williams & Wilkins; 1980
    [Google Scholar]
  33. Gordon RE, Barnett DA, Handerhan JE, Pang C-N. Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 1974; 24:54–63 [View Article]
    [Google Scholar]
  34. Williams ST, Goodfellow M, Alderson G, Wellington EM, Sneath PH et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983; 129:1743–1813 [View Article] [PubMed]
    [Google Scholar]
  35. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article] [PubMed]
    [Google Scholar]
  36. Saddler GS, Tavecchia P, Lociuro S, Zanol M, Colombo L et al. Analysis of madurose and other actinomycete whole cell sugars by gas chromatography. J Microbiol Methods 1991; 14:185–191 [View Article]
    [Google Scholar]
  37. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
    [Google Scholar]
  38. Minnikin DE, Alshamaony L, Goodfellow M. Differentiation of Mycobacterium, Nocardia, and related taxa by thin-layer chromatographic analysis of whole-organism methanolysates. J Gen Microbiol 1975; 88:200–204 [View Article] [PubMed]
    [Google Scholar]
  39. Embley TM, Wait R. Structural lipids of eubacteria. In Goodfellow M, O’Donnell AG. eds Chemical Methods in Prokaryotic Systematics England: John Wiley & Sons; 1994 pp 121–161
    [Google Scholar]
  40. Kroppenstedt RM. Fatty acid and menaquinone analysis of actinomycetes and related organisms. In Goodfellow M, Minnikin DE. eds Chemical Methods in Bacterial Systematics London: Academic Press; 1985 pp 173–199
    [Google Scholar]
  41. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:16
    [Google Scholar]
  42. Minnikin DE, Hutchinson IG, Caldicott AB, Goodfellow M. Thin-layer chromatography of methanolysates of mycolic acid-containing bacteria. J Chromatogr A 1980; 188:221–233 [View Article]
    [Google Scholar]
  43. Linos A, Steinbüchel A, Spröer C, Kroppenstedt RM. Gordonia polyisoprenivorans sp. nov., a rubber-degrading actinomycete isolated from an automobile tyre. Int J Syst Bacteriol 1999; 49 Pt 4:1785–1791 [View Article] [PubMed]
    [Google Scholar]
  44. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  45. 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] [PubMed]
    [Google Scholar]
  46. 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]
  47. 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] [PubMed]
    [Google Scholar]
  48. Zhu W-Z, Ge Y-M, Gao H-M, Dai J, Zhang X-L 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] [PubMed]
    [Google Scholar]
  49. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB et al. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 2020; 70:2782–2858 [View Article]
    [Google Scholar]
  50. Torres M, Balcells M, Sala N, Sanchis V, Canela R. Bactericidal and fungicidal activity of Aspergillus ochraceus metabolites and some derivatives. Pestic Sci 1998; 53:9–14 [View Article]
    [Google Scholar]
  51. Hornemann U, Hurley LH, Speedie MK, Guenther HF, Floss HG. Biosynthesis of the antibiotic indolmycin by Streptomyces griseus. C-methylation at the β-carbon atom of the tryptophan side-chain. J Chem Soc D 1969; 0:245–246 [View Article]
    [Google Scholar]
  52. Anke T, Oberwinkler F, Steglich W, Schramm G. The strobilurins - new antifungal antibiotics from the basidiomycete Strobilurus tenacellus. J Antibiot 1977; 30:806–810 [View Article]
    [Google Scholar]
  53. Wright W, Little J, Liu F, Chakraborty R. Isolation and structural identification of the trihydroxamate siderophore vicibactin and its degradative products from Rhizobium leguminosarum ATCC 14479 bv. trifolii. Biometals 2013; 26:271–283 [View Article] [PubMed]
    [Google Scholar]
  54. Santos-Aberturas J, Vior NM. Beyond soil-dwelling actinobacteria: fantastic antibiotics and where to find them. Antibiotics 2022; 11:195 [View Article] [PubMed]
    [Google Scholar]
  55. Prosperini A, Berrada H, Ruiz MJ, Caloni F, Coccini T et al. A review of the mycotoxin enniatin B. Front Public Health 2017; 5:304 [View Article] [PubMed]
    [Google Scholar]
  56. Huang H, Yao Y, He Z, Yang T, Ma J et al. Antimalarial β-carboline and indolactam alkaloids from Marinactinospora thermotolerans, a deep sea isolate. J Nat Prod 2011; 74:2122–2127 [View Article] [PubMed]
    [Google Scholar]
  57. Klapper M, Götze S, Barnett R, Willing K, Stallforth P. Bacterial alkaloids prevent amoebal predation. Angew Chem Int Ed Engl 2016; 55:8944–8947 [View Article] [PubMed]
    [Google Scholar]
  58. Wang X, Zhou H, Chen H, Jing X, Zheng W et al. Discovery of recombinases enables genome mining of cryptic biosynthetic gene clusters in Burkholderiales species. Proc Natl Acad Sci U S A 2018; 115:E4255–E4263 [View Article] [PubMed]
    [Google Scholar]
  59. Chaudhary DK, Kim J. Rhodococcus olei sp. nov., with the ability to degrade petroleum oil, isolated from oil-contaminated soil. Int J Syst Evol Microbiol 2018; 68:1749–1756 [View Article] [PubMed]
    [Google Scholar]
  60. Yassin AF. Rhodococcus triatomae sp. nov., isolated from a blood-sucking bug. Int J Syst Evol Microbiol 2005; 55:1575–1579 [View Article] [PubMed]
    [Google Scholar]
  61. Bernard KA, Funke G. Genus Corynebacterium Lehmann and Neumann 1896, 350AL emend. Bernard, Weibe, Burze, Reimer, Ng, Singh, Schindle and Pacheco 2010, 877. In Goodfellow M, Kämpfer P, Hussse H-J, Trujilo M, Suzuki K-I et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 245–289
    [Google Scholar]
  62. Cheng J, Wang H-F, Li L, Chen W, Duan Y-Q et al. Tomitella cavernea sp. nov., an actinomycete isolated from soil. Int J Syst Evol Microbiol 2014; 64:2319–2323 [View Article] [PubMed]
    [Google Scholar]
  63. Goodfellow M, Kumar Y. Genus Tsukamurella Collins, Smida, Dorsch and Stackebrandt 1988, 387AP. In Kämpfer P et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 500–509
    [Google Scholar]
  64. Han C, Liu T, Guo L, Wang X, Zhao J et al. Description of Jidongwangia harbinensis gen nov. sp. nov. Int J Syst Evol Microbiol 2023; 73:5670 [PubMed]
    [Google Scholar]
  65. Miyanishi M, Hamada M, Taniguchi T, Enomoto N, Oota T et al. Lolliginicoccus levis gen. nov., sp. nov., a novel bacterium isolated from the brain of the Chiroteuthis picteti squid, and reclassification of two Hoyosella species as Lolliginicoccus suaedae comb. nov. and Lolliginicoccus lacisalsi comb. nov. Int J Syst Evol Microbiol 2023; 73:5788
    [Google Scholar]
  66. Rainey FA. Genus Dietzia Rainey, Klatte, Kroppenstedt and Stackebrandt 1995 33VP emend. Kämpfer, Langer, Martin, Jäckel and Busse 2010, 394VP. In Goodfellow M, Kämpfer P, Hussse H-J, Trujilo M, Suzuki K-I et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 301–311
    [Google Scholar]
  67. Goodfellow M. Family Nocardiaceae (Castellani and Charmers 1919) emend. Zhi, Li and Stackebrandt 2009. In Goodfellow M, Kämpfer P, Hussse H-J, Trujilo M, Suzuki K-I et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 376–496
    [Google Scholar]
  68. Magee JG, Ward AC. Genus Mycobacterium Lehmann and Neumann 1896, 363AL. In Goodfellow M, Kämpfer P, Hussse H-J, Trujilo M, Suzuki K-I et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 312–375
    [Google Scholar]
  69. Wang Y-X, Wang H-B, Zhang Y-Q, Xu L-H, Jiang C-L et al. Rhodococcus kunmingensis sp. nov., an actinobacterium isolated from a rhizosphere soil. Int J Syst Evol Microbiol 2008; 58:1467–1471 [View Article] [PubMed]
    [Google Scholar]
  70. Butler WA. Genus Segniliparus Butler, Floyd, Brown, Toney, Daneshvar, Cooksey, Carr, Steigerwalt and Charles 2005, 1621VP. In Goodfellow M, Kämpfer P, Hussse H-J, Trujilo M, Suzuki K-I et al. eds Bergey’s Manual of Systematic Bacteriology vol 5 New York: Springer; 2012 pp 497–499
    [Google Scholar]
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