1887
  1. Home
  2. Publications
  3. International Journal of Systematic and Evolutionary Microbiology
  4. Volume 67, Issue 12
  5. Article

f Two novel species of rapidly growing mycobacteria: Mycobacterium lehmannii sp. nov. and Mycobacterium neumannii sp. nov.

PDF
252.78 Kb
HTML
89.03 Kb
  • Received:
  • Accepted:
  • Cover date:
Preview this:
Free Preview thumbnail Magnify
Zoom in
Zoomout

Two novel species of rapidly growing mycobacteria: Mycobacterium lehmannii sp. nov. and Mycobacterium neumannii sp. nov., Page 1 of 1

| /docserver/preview/fulltext/ijsem/67/12/4948_ijsem002350-1.gif

  • Two rapidly growing mycobacteria with identical 16S rRNA gene sequences were the subject of a polyphasic taxonomic study. The strains formed a well-supported subclade in the mycobacterial 16S rRNA gene tree and were most closely associated with the type strain of Mycobacterium novocastrense . Single and multilocus sequence analyses based on hsp65, rpoB and 16S rRNA gene sequences showed that strains SN 1900 and SN 1904 are phylogenetically distinct but share several chemotaxonomic and phenotypic features that are are consistent with their classification in the genus Mycobacterium . The two strains were distinguished by their different fatty acid and mycolic acid profiles, and by a combination of phenotypic features. The digital DNA–DNA hybridization (dDDH) and average nucleotide identity (ANI) values for strains SN 1900 and SN 1904 were 61.0 % and 94.7 %, respectively; in turn, the corresponding dDDH and ANI values with M. novocastrense DSM 44203 were 41.4 % and 42.8 % and 89.3 % and 89.5 %, respectively. These results show that strains SN1900 and SN 1904 form new centres of taxonomic variation within the genus Mycobacterium . Consequently, strains SN 1900 (40=CECT 8763=DSM 43219) and SN 1904 (2409=CECT 8766=DSM 43532) are considered to represent novel species, for which the names Mycobacterium lehmannii sp. nov. and Mycobacterium neumannii sp. nov. are proposed. A strain designated as ‘ Mycobacterium acapulsensis’ was shown to be a bona fide member of the putative novel species, M. lehmannii.

  • The GenBank accession numbers of strains SN 1900 and SN 1904 for 16S rRNA, hsp65, rpoB gene sequences and genomes are KY933300, KY933786 and KY933788 and KY933299, KY933787 and KY933789, respectively. The genome accession numbers of strains SN 1900 and SN 1904 are NKCN00000000 and NKCO00000000, respectively.

  • One supplementary figure is available with the online version of this article.

© 2017 IUMS | Published by the Microbiology Society

  • 1. Lehmann KB, Neumann R. Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik München: 1896
    [Google Scholar]
  • 2. Chester FD. Report of mycologist: bacteriological work. Del Agric Exp Sta Bull 1897; 9: 38– 145
    [Google Scholar]
  • 3. Magee JG, Ward AC. Genus I. Mycobacterium. In Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI. et al. (editors) Bergey's Manual of Systematics Bacteriology, 2nd ed.vol. 5 The Actinobacteria New York: Springer; 2012; pp. 312– 375
    [Google Scholar]
  • 4. Forbes BA. Mycobacterial taxonomy. J Clin Microbiol 2017; 55: 380– 383 [CrossRef] [PubMed]
    [Google Scholar]
  • 5. Parte AC. LPSN-list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 2014; 42: D613– D616 [CrossRef] [PubMed]
    [Google Scholar]
  • 6. Wayne LG, Kubica GP. The mycobacteria. In Sneath PHA, Mair NS, Sharpe ME, Holt JG. (editors) Bergey's Manual of Systematics Bacteriologyvol. 2 Baltimore: Williams & Wilkins; 1986; pp. 1435– 1457
    [Google Scholar]
  • 7. Ben Salah I, Cayrou C, Raoult D, Drancourt M. Mycobacterium marseillense sp. nov., Mycobacterium timonense sp. nov. and Mycobacterium bouchedurhonense sp. nov., members of the Mycobacterium avium complex. Int J Syst Evol Microbiol 2009; 59: 2803– 2808 [CrossRef] [PubMed]
    [Google Scholar]
  • 8. Lee SY, Kim BJ, Kim H, Won YS, Jeon CO et al. Mycobacterium paraintracellulare sp. nov., for the genotype INT-1 of Mycobacterium intracellulare. Int J Syst Evol Microbiol 2016; 66: 3132– 3141 [CrossRef] [PubMed]
    [Google Scholar]
  • 9. Tortoli E, Kohl TA, Brown-Elliott BA, Trovato A, Leão SC et al. Emended description of Mycobacterium abscessus, Mycobacterium abscessus subsp. abscessus and Mycobacterium abscessus subsp. bolletii and designation of Mycobacterium abscessus subsp. massiliense comb. nov. Int J Syst Evol Microbiol 2016; 66: 4471– 4479 [CrossRef] [PubMed]
    [Google Scholar]
  • 10. Ramaprasad EV, Rizvi A, Banerjee S, Sasikala C, Ramana CV. Mycobacterium oryzae sp. nov., a scotochromogenic, rapidly growing species is able to infect human macrophage cell line. Int J Syst Evol Microbiol 2016; 66: 4530– 4536 [CrossRef] [PubMed]
    [Google Scholar]
  • 11. Tran PM, Dahl JL. Mycobacterium sarraceniae sp. nov. and Mycobacterium helvum sp. nov., isolated from the pitcher plant Sarracenia purpurea. Int J Syst Evol Microbiol 2016; 66: 4480– 4485 [CrossRef] [PubMed]
    [Google Scholar]
  • 12. Fedrizzi T, Meehan CJ, Grottola A, Giacobazzi E, Fregni Serpini G et al. Genomic characterization of nontuberculous mycobacteria. Sci Rep 2017; 7: 45258 [CrossRef] [PubMed]
    [Google Scholar]
  • 13. Bojalil LF, Cerbon J, Trujillo A. Adansonian classification of mycobacteria. J Gen Microbiol 1962; 28: 333– 346 [CrossRef] [PubMed]
    [Google Scholar]
  • 14. Shojaei H, Goodfellow M, Magee JG, Freeman R, Gould FK et al. Mycobacterium novocastrense sp. nov., a rapidly growing photochromogenic mycobacterium. Int J Syst Bacteriol 1997; 47: 1205– 1207 [CrossRef] [PubMed]
    [Google Scholar]
  • 15. Jensen KA. Reinzuechtung und Typenbestimmung von Tuberkelbazillenstämmen. Zentralbl Bakteriol I. Orig 1932; 125: 222– 239
    [Google Scholar]
  • 16. Lorian V. Differentiation of Mycobacterium tuberculosis and Runyon group 3 "V" strains on direct cord-reading agar. Am Rev Respir Dis 1968; 97: 1133– 1135 [CrossRef] [PubMed]
    [Google Scholar]
  • 17. MacFaddin JF. Media for Isolation–Cultivation–Identification–Maintenance of Medical Bacteria Baltimore: Williams & Wilkins; 1985
    [Google Scholar]
  • 18. Runyon EH, Karlson AG, Kubica GP, Wayne LG. Mycobacterium Washington, DC: American Society for Microbiology; 1980
    [Google Scholar]
  • 19. Amaro A, Duarte E, Amado A, Ferronha H, Botelho A. Comparison of three DNA extraction methods for Mycobacterium bovis, Mycobacterium tuberculosis and Mycobacterium avium subsp. avium. Lett Appl Microbiol 2008; 47: 8– 11 [CrossRef] [PubMed]
    [Google Scholar]
  • 20. Sangal V, Jones AL, Goodfellow M, Hoskisson PA, Kämpfer P et al. Genomic analyses confirm close relatedness between Rhodococcus defluvii and Rhodococcus equi (Rhodococcus hoagii). Arch Microbiol 2015; 197: 113– 116 [CrossRef] [PubMed]
    [Google Scholar]
  • 21. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19: 455– 477 [CrossRef] [PubMed]
    [Google Scholar]
  • 22. Yoon SH, Ha SM, 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 [CrossRef] [PubMed]
    [Google Scholar]
  • 23. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14: 60 [CrossRef] [PubMed]
    [Google Scholar]
  • 24. Meier-Kolthoff JP, Göker M, Spröer C, Klenk HP. When should a DDH experiment be mandatory in microbial taxonomy?. Arch Microbiol 2013; 195: 413– 418 [CrossRef] [PubMed]
    [Google Scholar]
  • 25. 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 [CrossRef] [PubMed]
    [Google Scholar]
  • 26. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32: 1792– 1797 [CrossRef] [PubMed]
    [Google Scholar]
  • 27. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312– 1313 [CrossRef] [PubMed]
    [Google Scholar]
  • 28. Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010; 17: 337– 354 [CrossRef] [PubMed]
    [Google Scholar]
  • 29. Goloboff PA, Farris JS, Nixon KC. TNT, a free program for phylogenetic analysis. Cladistics 2008; 24: 774– 786 [CrossRef]
    [Google Scholar]
  • 30. Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 Sunderland: Sinauer Associates; 2002
    [Google Scholar]
  • 31. McNabb A, Eisler D, Adie K, Amos M, Rodrigues M et al. Assessment of partial sequencing of the 65-kilodalton heat shock protein gene (hsp65) for routine identification of Mycobacterium species isolated from clinical sources. J Clin Microbiol 2004; 42: 3000– 3011 [CrossRef] [PubMed]
    [Google Scholar]
  • 32. 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 [CrossRef] [PubMed]
    [Google Scholar]
  • 33. Tsukamura M, Yano I, Imaeda T. Mycobacterium moriokaense sp. nov., a rapidly growing, nonphotochromogenic Mycobacterium. Int J Syst Bacteriol 1986; 36: 333– 338 [CrossRef]
    [Google Scholar]
  • 34. Shahraki AH, Çavuşoğlu C, Borroni E, Heidarieh P, Koksalan OK et al. Mycobacterium celeriflavum sp. nov., a rapidly growing scotochromogenic bacterium isolated from clinical specimens. Int J Syst Evol Microbiol 2015; 65: 510– 515 [CrossRef] [PubMed]
    [Google Scholar]
  • 35. Tsukamura M. Adansonian classification of mycobacteria. J Gen Microbiol 1966; 45: 253– 273 [CrossRef] [PubMed]
    [Google Scholar]
  • 36. Tortoli E, Piersimoni C, Kroppenstedt RM, Montoya-Burgos JI, Reischl U et al. Mycobacterium doricum sp. nov. Int J Syst Evol Microbiol 2001; 51: 2007– 2012 [CrossRef] [PubMed]
    [Google Scholar]
  • 37. Reischl U, Melzl H, Kroppenstedt RM, Miethke T, Naumann L et al. Mycobacterium monacense sp. nov. Int J Syst Evol Microbiol 2006; 56: 2575– 2578 [CrossRef] [PubMed]
    [Google Scholar]
  • 38. Bönicke R, Juhasz SE. Beschreibung der neuen species Mycobacterium vaccae n. sp. Zentralbl Bakteriol Parasitenkde Infektionskr Hyg Abt Orig 1964; 192: 133– 135
    [Google Scholar]
  • 39. Luquin M, Ausina V, Vincent-Levy-Frebault V, Laneelle MA, Belda F et al. Mycobacterium brumae sp. nov., a rapidly growing, nonphotochromogenic Mycobacterium. Int J Syst Bacteriol 1993; 43: 405– 413 [CrossRef]
    [Google Scholar]
  • 40. Richter E, Niemann S, Gloeckner FO, Pfyffer GE, Rüsch-Gerdes S. Mycobacterium holsaticum sp. nov. Int J Syst Evol Microbiol 2002; 52: 1991– 1996 [CrossRef] [PubMed]
    [Google Scholar]
  • 41. Lamy B, Marchandin H, Hamitouche K, Laurent F. Mycobacterium setense sp. nov., a Mycobacterium fortuitum-group organism isolated from a patient with soft tissue infection and osteitis. Int J Syst Evol Microbiol 2008; 58: 486– 490 [CrossRef] [PubMed]
    [Google Scholar]
  • 42. Kirschner P, Springer B, Vogel U, Meier A, Wrede A et al. Genotypic identification of mycobacteria by nucleic acid sequence determination: report of a 2-year experience in a clinical laboratory. J Clin Microbiol 1993; 31: 2882– 2889 [PubMed]
    [Google Scholar]
  • 43. Katahira K, Ogura Y, Gotoh Y, Hayashi T. Draft genome sequences of five rapidly growing Mycobacterium species, M. thermoresistibile, M. fortuitum subsp. acetamidolyticum, M. canariasense, M. brisbanense, and M. novocastrense. Genome Announc 2016; 4: e00322-16 [CrossRef] [PubMed]
    [Google Scholar]
  • 44. 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 [CrossRef] [PubMed]
    [Google Scholar]
  • 45. Aziz RK, Devoid S, Disz T, Edwards RA, Henry CS et al. SEED servers: high-performance access to the SEED genomes, annotations, and metabolic models. PLoS One 2012; 7: e48053 [CrossRef] [PubMed]
    [Google Scholar]
  • 46. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106: 19126– 19131 [CrossRef] [PubMed]
    [Google Scholar]
  • 47. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37: 463– 464 [CrossRef]
    [Google Scholar]
  • 48. 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 [CrossRef] [PubMed]
    [Google Scholar]
  • 49. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64: 316– 324 [CrossRef] [PubMed]
    [Google Scholar]
  • 50. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28: 226– 231 [PubMed]
    [Google Scholar]
  • 51. Collins MD. 11 Analysis of isoprenoid quinones. Meth Microbiol 1985; 18: 329– 366 [Crossref]
    [Google Scholar]
  • 52. Kroppenstedt RM. Fatty acid and menaquinone analysis of actinomycetes and related organisms. In Goodfellow M, Minnikin DE. (editors) Chemical Methods in Bacterial Systematics London: Academic Press; 1985; pp. 173– 199
    [Google Scholar]
  • 53. Lechavalier MP, Lechevalier HA. Composition of whole-cell hydrolysates as a criterion in the classification of aerobic actinomycetes. In Prauser H. (editor) The Actinomycetales Jena: Gustav Fischer Verlag; 1970; pp. 311– 316
    [Google Scholar]
  • 54. 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 [CrossRef]
    [Google Scholar]
  • 55. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16: 584– 586 [PubMed]
    [Google Scholar]
  • 56. Kuykendall LD, Roy MA, O'Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 1988; 38: 358– 361 [CrossRef]
    [Google Scholar]
  • 57. Sasser MJ. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, Technical Note 101, Microbial ID. Newark, USA: Del Inc; 1990
    [Google Scholar]
  • 58. Minnikin DE, Goodfellow M. Lipid composition in the classification and identification of nocardiae and related taxa. In Goodfellow M, Brownell GH, Serrano JA. (editors) The Biology of the Nocardiae London: Academic Press; 1976; pp. 160– 219
    [Google Scholar]
  • 59. Teramoto K, Suga M, Sato T, Wada T, Yamamoto A et al. Characterization of mycolic acids in total fatty acid methyl ester fractions from Mycobacterium species by high resolution MALDI-TOFMS. Mass Spectrom 2015; 4: A0035 [CrossRef] [PubMed]
    [Google Scholar]
  • 60. Nouioui I, Carro L, Teramoto K, Igual JM, Jando M et al. Mycobacterium eburneum sp. nov., a non-chromogenic, fast-growing strain isolated from sputum. Int J Syst Evol Microbiol 2017; 67: 3174– 3181 [CrossRef] [PubMed]
    [Google Scholar]
  • 61. Tomioka H, Saito H, Sato K, Dawson DJ. Arylsulfatase activity for differentiating Mycobacterium avium and Mycobacterium intracellulare. J Clin Microbiol 1990; 28: 2104– 2106 [PubMed]
    [Google Scholar]
  • 62. Palomino JC, Leão SC, Ritacco V. 2007; Tuberculosis 2007 – From basic science to patient care. www.Tuberculosistextbook.com
  • 63. Sequeira de Latini MD, Barrera L. Manual para el Diagnóstico Bacteriológico de la Tuberculosis: Normas y Guía Técnica. Parte I Baciloscopía. Organización Panamericana de la Salud 2008
  • 64. Kent PT, Kubica GP. Public Health Mycobacteriology: A Guide for the Level III Laboratory Atlanta, GA: Centers for Disease control and Prevention; 1985
    [Google Scholar]
  • 65. Bernardelli A. Manual de procedimientos. Clasificación fenotípica de las micobacterias: Dirección de Laboratorio y Control Técnico 2007
    [Google Scholar]
  • 66. Kilburn JO, Silcox VA, Kubica GP. Differential identification of mycobacteria. V. The tellurite reduction test. Am Rev Respir Dis 1969; 99: 94– 100 [CrossRef] [PubMed]
    [Google Scholar]
  • 67. Ribón W. chemical isolation and identification of mycobacteria. In Jimenez-Lopez JC. (editor) Biochemical testing: InTech 2012
    [Google Scholar]
  • 68. Vaas LA, Sikorski J, Hofner B, Fiebig A, Buddruhs N et al. opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics 2013; 29: 1823– 1824 [CrossRef] [PubMed]
    [Google Scholar]
  • 69. Vaas LA, Sikorski J, Michael V, Göker M, Klenk HP. Visualization and curve-parameter estimation strategies for efficient exploration of phenotype microarray kinetics. PLoS One 2012; 7: e34846 [CrossRef] [PubMed]
    [Google Scholar]
  • 70. Asmar S, Rascovan N, Robert C, Drancourt M. Draft genome sequence of Mycobacterium acapulcensis strain CSURP1424. Genome Announc 2016; 4: e00836-16 [CrossRef] [PubMed]
    [Google Scholar]
  • 71. Parker CT, Tindall BJ, Garrity GM. International code of Nomenclature of Prokaryotes code (2008 version). Int J Syst Evol Microbial 2015; doi:10.1099:ijsem.0000778
    [Google Scholar]
http://sgm.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002350
Loading

Supplementary Data

 Data loading....

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002350
2017-10-23
2019-02-18
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/12/4948.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002350&mimeType=html&fmt=ahah

Author and Article Information

 Figure data loading....

Footnotes:

Validated antibodies in this article

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error