1887

Abstract

A nonmotile, facultatively anaerobic and rod-shaped bacterial strain, designated M1 was isolated from a bioreactor being operated at pH ~2 at Brisbane, Australia. Colonies appeared to be convex and white. Phylogenetic analysis of its genome revealed an affiliation with the genus and its closest species based on 16S rRNA gene analysis were DSM 45454 (98.8 % similarity) and CIP 104321 (98.8 %) with which strain M1 shared average nucleotide identity of 81.2 % and digital DNA–DNA hybridization similarity of 23.8 %. Strain M1 grew optimally at 0 % NaCl, at pH 6 and at between 30–33 °C. The polar lipid profile of strain M1 consisted of diphosphatidylglycerol, aminophosphoglycolipid, phosphatidylcholine, phospholipid, aminolipid, phosphoglyolipid, phosphatidylglycerol, two unidentified glycolipids and four unidentified lipids. The dominant cellular fatty acids (>10 %) were C and C 9 and summed feature 7 (C 7 and/or C 6). The DNA G+C content of strain M1 was 69.1 mol%. Based on phylogenomic analysis coupled with physiological and chemotaxonomic characterizations, we classify strain M1 as representing a novel species within the genus , for which the name nov. is proposed. The type strain is M1 (=MCCC 1H00416=KCTC 49392).

Funding
This study was supported by the:
  • University of Queensland Research Training Scholarship
    • Principle Award Recipient: JunXia
  • Advance Queensland Industry Research Fellowships (Award RM2019002600)
    • Principle Award Recipient: NiGaofeng
  • Australian Research Council (Award DP180103595)
    • Principle Award Recipient: ShihuHu
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-06-09
2024-04-29
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References

  1. Hartmans S, Bont JAM, Stackebrandt E. Chapter 1.1.18-The genus Mycobacterium-nonmedical. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes: Volume 3: Archaea. Bacteria: Firmicutes, Actinomycetes New York, NY: Springer New York; 2006 pp 889–918
    [Google Scholar]
  2. Brzostek A, Pawelczyk J, Rumijowska-Galewicz A, Dziadek B, Dziadek J et al. Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J Bacteriol 2009; 191:6584–6591 [View Article] [PubMed]
    [Google Scholar]
  3. Falkinham JO. Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 2009; 107:356–367 [View Article] [PubMed]
    [Google Scholar]
  4. Tortoli E. Phylogeny of the genus Mycobacterium: many doubts, few certainties. Infect Genet Evol 2012; 12:827–831 [View Article] [PubMed]
    [Google Scholar]
  5. Magee GM, Ward AC et al. Genus I. Mycobacterium Lehmann and Neumann 1896, 363AL. In Goodfellow M, Kampfer P, Busse HJ, Trujillo ME, Suzuki K. eds Bergey’s Manual of Systematic Bacteriology, Vol. 5, Actinobacteria New York, NY: Springer; 2012 pp 312–375
    [Google Scholar]
  6. Tsukamura M. Identification of mycobacteria. Tubercle 1967; 48:311–338 [View Article] [PubMed]
    [Google Scholar]
  7. Wayne LG, Kubica GP. Genus Mycobacterium. In Sneath M, Sharpe H. eds Bergey’s Manual of Systematic Bacteriology vol 2 Williams & Wilkins, Baltimore: 1986 pp 1436–1457
    [Google Scholar]
  8. Kim SH, Shin JH. Identification of nontuberculous mycobacteria using multilocous sequence analysis of 16S rRNA, hsp65, and rpoB. J Clin Lab Anal 2018; 32: [View Article] [PubMed]
    [Google Scholar]
  9. 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] [PubMed]
    [Google Scholar]
  10. Brown CT, Hug LA, Thomas BC, Sharon I, Castelle CJ et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 2015; 523:208–211 [View Article] [PubMed]
    [Google Scholar]
  11. Tonini J, Moore A, Stern D, Shcheglovitova M, Ortí G et al. Concatenation and species tree methods exhibit statistically indistinguishable accuracy under a range of simulated condSpecies Tree Methods Exhibit Statistically Indistinguishable Accuracy under a Range of Simulated Conditions. PLoS Curr 2015; 7:ecurrents.tol.34260cc27551a527b124ec5f6334b6be [View Article] [PubMed]
    [Google Scholar]
  12. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al. A new view of the tree of life. Nat Microbiol 2016; 1:16048 [View Article] [PubMed]
    [Google Scholar]
  13. Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K et al. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 2018; 68:2386–2392 [View Article] [PubMed]
    [Google Scholar]
  14. 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]
  15. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005; 102:2567–2572 [View Article] [PubMed]
    [Google Scholar]
  16. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S et al. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  17. Olm MR, Crits-Christoph A, Diamond S, Lavy A, Matheus Carnevali PB et al. Consistent metagenome-derived metrics verify and delineate bacterial species boundaries. mSystems 2020; 5:e00731-19 [View Article] [PubMed]
    [Google Scholar]
  18. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH, Hancock J. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019; 36:1925–1927 [View Article]
    [Google Scholar]
  19. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
    [Google Scholar]
  20. Glaeser SP, Kämpfer P. Multilocus sequence analysis (MLSA) in prokaryotic taxonomy. Syst Appl Microbiol 2015; 38:237–245 [View Article] [PubMed]
    [Google Scholar]
  21. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article] [PubMed]
    [Google Scholar]
  22. Vandamme P, Peeters C. Time to revisit polyphasic taxonomy. Antonie van Leeuwenhoek 2014; 106:57–65 [View Article] [PubMed]
    [Google Scholar]
  23. Ringuet H, Akoua-Koffi C, Honore S, Varnerot A, Vincent V et al. hsp65 sequencing for identification of rapidly growing mycobacteria. J Clin Microbiol 1999; 37:852–857 [View Article] [PubMed]
    [Google Scholar]
  24. Lee H, Park HJ, Cho SN, Bai GH, Kim SJ. Species identification of mycobacteria by PCR-restriction fragment length polymorphism of the rpoB gene. J Clin Microbiol 2000; 38:2966–2971 [View Article] [PubMed]
    [Google Scholar]
  25. Moore WEC, Stackebrandt E, Kandler O, Colwell RR, Krichevsky MI et al. Report of the Ad Hoc Committee on Reconciliation of Approaches to Bacterial Systematics. Int J Syst Bacteriol 1987; 37:463–464 [View Article]
    [Google Scholar]
  26. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article] [PubMed]
    [Google Scholar]
  27. Auch AF, von Jan M, Klenk H-P, Göker M et al. 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]
  28. Riojas MA, McGough KJ, Rider-Riojas CJ, Rastogi N, Hazbón MH. Phylogenomic analysis of the species of the Mycobacterium tuberculosis complex demonstrates that Mycobacterium africanum, Mycobacterium bovis, Mycobacterium caprae, Mycobacterium microti and Mycobacterium pinnipedii are later heterotypic synonyms of Mycobacterium tuberculosis. Int J Syst Evol Microbiol 2018; 68:324–332 [View Article] [PubMed]
    [Google Scholar]
  29. Delbès C, Moletta R, Godon JJ. Monitoring of activity dynamics of an anaerobic digester bacterial community using 16S rRNA polymerase chain reaction–single-strand conformation polymorphism analysis. Environ Microbiol 2000; 2:506–515 [View Article] [PubMed]
    [Google Scholar]
  30. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012; 62:716–721 [View Article] [PubMed]
    [Google Scholar]
  31. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  32. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J et al. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  33. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  34. 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]
  35. 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]
  36. Meehan CJ, Barco RA, Loh Y-H, Cogneau S, Rigouts L. Reconstituting the genus Mycobacterium. Int J Syst Evol Microbiol 2021; 71:004922 [View Article]
    [Google Scholar]
  37. Coombes BK, Brown NF, Valdez Y, Brumell JH, Finlay BB. Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J Biol Chem 2004; 279:49804–49815 [View Article] [PubMed]
    [Google Scholar]
  38. Gallant JL, Viljoen AJ, van Helden PD, Wiid IJF. Glutamate dehydrogenase is required by Mycobacterium bovis BCG for resistance to cellular stress. PLoS One 2016; 11:e0147706 [View Article] [PubMed]
    [Google Scholar]
  39. Pennacchietti E, D’Alonzo C, Freddi L, Occhialini A, De Biase D. The glutaminase-dependent acid resistance system: qualitative and quantitative assays and analysis of its distribution in enteric bacteria. Front Microbiol 2018; 9:2869 [View Article] [PubMed]
    [Google Scholar]
  40. Hayatsu M, Tago K, Uchiyama I, Toyoda A, Wang Y et al. An acid-tolerant ammonia-oxidizing γ-proteobacterium from soil. ISME J 2017; 11:1130–1141 [View Article] [PubMed]
    [Google Scholar]
  41. Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM et al. Methods for General and Molecular Microbiology, 3rd ed. Washington, DC, USA: American Society for Microbiology; 2007
    [Google Scholar]
  42. Koch R. Investigations of the Etiology of Wound Infections Connecticut: Greenwood Press; 1987
    [Google Scholar]
  43. Cowan ST, Steel KJ. Manual for the Identification of Medical Bacteria London: Cambridge University Press; 1965
    [Google Scholar]
  44. Smibert RM, Krieg NR. Phenotypic characterization. In Gerhardt P, Murray RGE, Wood WA, Krieg NR. eds Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1994 pp 607–654
    [Google Scholar]
  45. Holdeman LV, Cato EP, Moore WEC. Anaerobe Laboratory Manual, 4th edn. Blacksburg, VA: Virginia Polytechnic Institute and State University; 1977
    [Google Scholar]
  46. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids. MIDI Technical Note 101 Newark, DE: MIDI, Inc; 1990
    [Google Scholar]
  47. 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]
  48. Vilchèze C, Jacobs WRJ. Isolation and analysis of Mycobacterium tuberculosis mycolic acids. Curr Protoc Microbiol 2007; Chapter 10:10A [View Article] [PubMed]
    [Google Scholar]
  49. Sahraoui N, Ballif M, Zelleg S, Yousfi N, Ritter C et al. Mycobacterium algericum sp. nov., a novel rapidly growing species related to the Mycobacterium terrae complex and associated with goat lung lesions. Int J Syst Evol Microbiol 2011; 61:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  50. Mun H-S, Park J-H, Kim H, Yu H-K, Park Y-G et al. Mycobacterium senuense sp. nov., a slowly growing, non-chromogenic species closely related to the Mycobacterium terrae complex. Int J Syst Evol Microbiol 2008; 58:641–646 [View Article] [PubMed]
    [Google Scholar]
  51. Magee JG, Ward AC. Mycobacterium. In Whitman WB. eds Bergey’s Manual of Systematics of Archaea and Bacteria Wiley; 2015 pp 1–84
    [Google Scholar]
  52. Tortoli E, Gitti Z, Klenk HP, Lauria S, Mannino R et al. Survey of 150 strains belonging to the Mycobacterium terrae complex and description of Mycobacterium engbaekii sp. nov., Mycobacterium heraklionense sp. nov. and Mycobacterium longobardum sp. nov. Int J Syst Evol Microbiol 2013; 63:401–411 [View Article]
    [Google Scholar]
  53. Kazda J, Cooney R, Monaghan M, Quinn PJ, Stackebrandt E et al. Mycobacterium hiberniae sp. nov. Int J Syst Bacteriol 1993; 43:352–357 [View Article] [PubMed]
    [Google Scholar]
  54. Hannigan GD, Krivogorsky B, Fordice D, Welch JB, Dahl JL. Mycobacterium minnesotense sp. nov., a photochromogenic bacterium isolated from sphagnum peat bogs. Int J Syst Evol Microbiol 2013; 63:124–128 [View Article] [PubMed]
    [Google Scholar]
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