1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 56, Issue 1

gene sequence-based characterization of emerging non-tuberculous mycobacteria with descriptions of sp. nov., sp. nov. and sp. nov. Free

Abstract

Over the past 10 years, 16S rRNA gene sequencing has contributed to the establishment of more than 45 novel species of non-tuberculous mycobacteria and to the description of emerging mycobacterial infections. Cumulative experience has indicated that this molecular tool underestimates the diversity of this group and does not distinguish between all recognized mycobacterial taxa. In order to improve the recognition of emerging rapidly growing mycobacteria (RGM), gene sequencing has been developed. Our previous studies have shown that an RGM isolate is a member of a novel species if it exhibits >3 % sequence divergence in the gene from the type strains of established species. When applied to a collection of 59 clinical RGM isolates, gene sequencing revealed nine novel isolates (15·3 %) whereas only two isolates (3·4 %) were deemed to be novel by conventional 16S rRNA gene sequence analysis. A polyphasic approach, including biochemical tests, antimicrobial susceptibility analyses, , and gene sequence analysis, DNA G+C content determination and cell-wall fatty acid composition analysis, supported the evidence that these nine isolates represent three novel species. Whereas sp. nov. (type strain N4=CIP 108542=CCUG 50185) and sp. nov. (type strain U8=CIP 108543=CCUG 50186; group) were susceptible to most antibiotics, sp. nov. (type strain BD=CIP 108541=CCUG 50184; group) was resistant to the quinolones, tetracycline, macrolides and imipenem. Only was resistant to clarithromycin. These data illustrate that gene sequence-based identification is a powerful tool to characterize emerging RGM and mycobacterial infections and provides valuable help in differentiating RGM at both the intra- and interspecies level, thus contributing to a faster and more efficient diagnosis and epidemiological follow-up.

  • Published Online:
Keyword(s): MIC, minimum inhibitory concentrations , NTM, non-tuberculous mycobacteria and RGM, rapidly growing mycobacteria
© SGM
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.63969-0
2006-01-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/56/1/133.html?itemId=/content/journal/ijsem/10.1099/ijs.0.63969-0&mimeType=html&fmt=ahah

References

  1. Adékambi, T. & Drancourt, M.(2004). Dissection of phylogenetic relationships among 19 rapidly growing Mycobacterium species by 16S rRNA, hsp65, sodA, recA, and rpoB gene sequencing. Int J Syst Evol Microbiol 54, 2095–2105.[CrossRef] [Google Scholar]
  2. Adékambi, T., Colson, P. & Drancourt, M.(2003).rpoB-based identification of nonpigmented and late-pigmenting rapidly growing mycobacteria. J Clin Microbiol 41, 5699–5708.[CrossRef] [Google Scholar]
  3. Adékambi, T., Reynaud-Gaubert, M., Greub, G., Gevaudan, M.-J., La Scola, B., Raoult, D. & Drancourt, M.(2004). Amoebal co-culture of ‘Mycobacterium massiliense’ sp. nov. from the sputum of a patient with hemoptoic pneumonia. J Clin Microbiol 42, 5493–5501.[CrossRef] [Google Scholar]
  4. Anaissie, E. J., Penzak, S. R. & Dignani, M. C.(2002). The hospital water supply as a source of nosocomial infections: a plea for action. Arch Intern Med 162, 1483–1492.[CrossRef] [Google Scholar]
  5. Ashford, D. A., Kellerman, S., Yakrus, M., Brim, S., Good, R. C., Finelli, L., Jarvis, W. R. & McNeil, M. M.(1997). Pseudo-outbreak of septicaemia due to rapidly growing mycobacteria associated with extrinsic contamination of culture supplement. J Clin Microbiol 35, 2040–2042. [Google Scholar]
  6. Blackwood, K. S., He, C., Gunton, J., Turenne, C. Y., Wolfe, J. & Kabani, A. M.(2000). Evaluation of recA sequences for identification of Mycobacterium species. J Clin Microbiol 38, 2846–2852. [Google Scholar]
  7. Böddinghaus, B., Rogall, T., Flohr, T., Blöcker, H. & Böttger, E. C.(1990). Detection and identification of mycobacteria by amplification of rRNA. J Clin Microbiol 28, 1751–1759. [Google Scholar]
  8. Brown, B. A., Wallace, R. J., Jr, Onyi, G. O., De Rosas, V. & Wallace, R. J., III(1992). Activities of four macrolides, including clarithromycin, against Mycobacterium fortuitum, Mycobacterium chelonae, and M. chelonae-like organisms. Antimicrob Agents Chemother 36, 180–184.[CrossRef] [Google Scholar]
  9. Brown-Elliott, B. A. & Wallace, R. J., Jr(2002). Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev 15, 716–746.[CrossRef] [Google Scholar]
  10. Butler, W. R. & Kilburn, J. O.(1990). High-performance liquid chromatography patterns of mycolic acids as criteria for identification of Mycobacterium chelonae, Mycobacterium fortuitum, and Mycobacterium smegmatis. J Clin Microbiol 28, 2094–2098. [Google Scholar]
  11. Conville, P. S. & Witebsky, F. G.(1998). Variables affecting results of sodium chloride tolerance test for identification of rapidly growing mycobacteria. J Clin Microbiol 36, 1555–1559. [Google Scholar]
  12. Cooksey, R. C., de Waard, J. H., Yakrus, M. A., Rivera, I., Chopite, M., Toney, S. R., Morlock, G. P. & Butler, W. R.(2004).Mycobacterium cosmeticum sp. nov., a novel rapidly growing species isolated from a cosmetic infection and from a nail salon. Int J Syst Evol Microbiol 54, 2385–2391.[CrossRef] [Google Scholar]
  13. Covert, T. C., Rodgers, M. R., Reyes, A. L. & Stelma, G. N., Jr(1999). Occurrence of nontuberculous mycobacteria in environmental samples. Appl Environ Microbiol 65, 2492–2496. [Google Scholar]
  14. Dailloux, M., Laurain, C., Weber, M. & Hartemann, P. H.(1999). Water and nontuberculous mycobacteria. Water Res 33, 2219–2228.[CrossRef] [Google Scholar]
  15. Dauendorffer, J. N., Guillemin, I., Aubry, A., Truffot-Pernot, C., Sougakoff, W., Jarlier, V. & Cambau, E.(2003). Identification of mycobacterial species by PCR sequencing of quinolone resistance-determining regions of DNA gyrase genes. J Clin Microbiol 41, 1311–1315.[CrossRef] [Google Scholar]
  16. Drancourt, M., Bollet, C., Carlioz, A., Martelin, R., Gayral, J. P. & Raoult, D.(2000). 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38, 3623–3630. [Google Scholar]
  17. Ferguson, D. D., Gershman, K., Jensen, B., Arduino, M. J., Yakrus, M. A., Cooksey, R. C. & Srinivasan, A.(2004).Mycobacterium goodii infections associated with surgical implants at Colorado hospital. Emerg Infect Dis 10, 1868–1871. [Google Scholar]
  18. Fox, G. E., Wisotzkey, J. D. & Jurtshuk, P., Jr(1992). How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identification. Int J Syst Bacteriol 42, 166–170.[CrossRef] [Google Scholar]
  19. Griffith, D. E., Girard, W. M. & Wallace, R. J., Jr(1993). Clinical features of pulmonary disease caused by rapidly growing mycobacteria. An analysis of 154 patients. Am Rev Respir Dis 147, 1271–1278.[CrossRef] [Google Scholar]
  20. Grimont, P. A.(1988). Use of DNA reassociation in bacterial classification. Can J Microbiol 34, 541–546.[CrossRef] [Google Scholar]
  21. Kauppinen, J., Nousiainen, T., Jantunen, E., Mattila, R. & Katila, M. L.(1999). Hospital water supply as a source of disseminated Mycobacterium fortuitum infection in a leukemia patient. Infect Control Hosp Epidemiol 20, 343–345.[CrossRef] [Google Scholar]
  22. Kent, P. T. & Kubica, G. P.(1985). Public Health Mycobacteriology: a guide for the level III laboratory. US Department of Health and Human Services, publication no. (CDC) 86-8230. Atlanta, GA: Centers for Disease Control.
  23. Khamis, A., Colson, P., Raoult, D. & La Scola, B.(2003). Usefulness of rpoB gene sequencing for identification of Afipia and Bosea species, including a strategy for choosing discriminative partial sequences. Appl Environ Microbiol 69, 6740–6749.[CrossRef] [Google Scholar]
  24. Kim, B. J., Lee, S. H., Lyu, M. A. & 7 other authors(1999). Identification of mycobacterial species by comparative sequence analysis of the RNA polymerase gene (rpoB). J Clin Microbiol 37, 1714–1720. [Google Scholar]
  25. Kubica, G. P., Dye, W. E., Cohn, M. L. & Middlebrook, G.(1963). Sputum digestion and decontamination with N-acetyl-l-cysteine-sodium hydroxide for culture of mycobacteria. Am Rev Respir Dis 87, 775–779. [Google Scholar]
  26. Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M.(2001).mega2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.[CrossRef] [Google Scholar]
  27. Lai, K. K., Brown, B. A., Westerling, J. A., Fontecchio, S. A., Zhang, Y. & Wallace, R. J., Jr(1998). Long-term laboratory contamination by Mycobacterium abscessus resulting in two pseudo-outbreaks: recognition with the use of random amplified polymorphic DNA (RAPD) polymerase chain reaction. Clin Infect Dis 27, 169–175.[CrossRef] [Google Scholar]
  28. La Scola, B., Zeaiter, Z., Khamis, A. & Raoult, D.(2003). Gene-sequence-based criteria for species definition in bacteriology: the Bartonella paradigm. Trends Microbiol 11, 318–321.[CrossRef] [Google Scholar]
  29. Lee, H., Bang, H. E., Bai, G. H. & Cho, S. N.(2003). Novel polymorphic region of the rpoB gene containing Mycobacterium species-specific sequences and its use in identification of mycobacteria. J Clin Microbiol 41, 2213–2218.[CrossRef] [Google Scholar]
  30. Maniu, C. V., Hellinger, W. C., Chu, S. Y., Palmer, R. & Alvarez-Elcoro, S.(2001). Failure of treatment for chronic Mycobacterium abscessus meningitis despite adequate clarithromycin levels in cerebrospinal fluid. Clin Infect Dis 33, 745–748.[CrossRef] [Google Scholar]
  31. Mesbah, M., Premachandran, U. & Whitman, W. B.(1989). Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39, 159–167.[CrossRef] [Google Scholar]
  32. Munoz, M., Julian, E., Garcia-Barcelo, M., Ausina, V. & Luquin, M.(1997). Easy differentiation of Mycobacterium mucogenicum from other species of the Mycobacterium fortuitum complex by thin-layer and gas chromatography of fatty esters and alcohols. J Chromatogr B Biomed Sci Appl 689, 341–347.[CrossRef] [Google Scholar]
  33. NCCLS(2002). Performance standards for antimicrobial susceptibility testing. Twelfth Informational Supplement, M100-S12. Wayne, PA: NCCLS.
  34. NCCLS(2003). Susceptibility testing of Mycobacteria, Nocardia, and other aerobic actinomycetes. Approved standard M24-A. Wayne, PA: NCCLS.
  35. Ninet, B., Monod, M., Emler, S., Pawlowski, J., Metral, C., Rohner, P., Auckenthaler, R. & Hirschel, B.(1996). Two different 16S rRNA genes in a mycobacterial strain. J Clin Microbiol 34, 2531–2536. [Google Scholar]
  36. Park, H., Jang, H., Kim, C., Chung, B., Chang, C. L., Park, S. K. & Song, S.(2000). Detection and identification of mycobacteria by amplification of the internal transcribed spacer regions with genus- and species-specific PCR primers. J Clin Microbiol 38, 4080–4085. [Google Scholar]
  37. Pauls, R. J., Turenne, C. Y., Wolfe, J. N. & Kabani, A.(2003). A high proportion of novel mycobacteria species identified by 16S rDNA analysis among slowly growing AccuProbe-negative strains in a clinical setting. Am J Clin Pathol 120, 560–566.[CrossRef] [Google Scholar]
  38. Reischl, U., Feldmann, K., Naumann, L., Gaugler, B. J., Ninet, B., Hirschel, B. & Emler, S.(1998). 16S rRNA sequence diversity in Mycobacterium celatum strains caused by presence of two different copies of 16S rRNA gene. J Clin Microbiol 36, 1761–1764. [Google Scholar]
  39. Ringuet, H., Akoua-Koffi, C., Honore, S., Varnerot, A., Vincent, V., Berche, P., Gaillard, J. L. & Pierre-Audigier, C.(1999).hsp65 sequencing for identification of rapidly growing mycobacteria. J Clin Microbiol 37, 852–857. [Google Scholar]
  40. Rogall, T., Flohr, T. & Böttger, E. C.(1990). Differentiation of Mycobacterium species by direct sequencing of amplified DNA. J Gen Microbiol 136, 1915–1920.[CrossRef] [Google Scholar]
  41. Sanguinetti, M., Ardito, F., Fiscarelli, E., La Sorda, M., D'Argenio, P., Ricciotti, G. & Fadda, G.(2001). Fatal pulmonary infection due to multidrug-resistant Mycobacterium abscessus in a patient with cystic fibrosis. J Clin Microbiol 39, 816–819.[CrossRef] [Google Scholar]
  42. Sasser, M.(1990).Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note no. 101. Newark, DE: MIDI.
  43. Schinsky, M. F., Morey, R. E., Steigerwalt, A. G. & 10 other authors(2004). Taxonomic variation in the Mycobacterium fortuitum third biovariant complex: description of Mycobacterium boenickei sp. nov., Mycobacterium houstonense sp. nov., Mycobacterium neworleansense sp. nov. and Mycobacterium brisbanense sp. nov. and recognition of Mycobacterium porcinum from human clinical isolates. Int J Syst Evol Microbiol 54, 1653–1667.[CrossRef] [Google Scholar]
  44. Smith, M. B., Schnadig, V. J., Boyars, M. C. & Woods, G. L.(2001). Clinical and pathologic features of Mycobacterium fortuitum infections. An emerging pathogen in patients with AIDS. Am J Clin Pathol 116, 225–232.[CrossRef] [Google Scholar]
  45. Soini, H. & Viljanen, M. K.(1997). Diversity of the 32-kilodalton protein gene may form a basis for species determination of potentially pathogenic mycobacterial species. J Clin Microbiol 35, 769–773. [Google Scholar]
  46. Springer, B., Stockman, L., Teschner, K., Roberts, G. D. & Böttger, E. C.(1996). Two-laboratory collaborative study on identification of mycobacteria: molecular versus phenotypic methods. J Clin Microbiol 34, 296–303. [Google Scholar]
  47. Stackebrandt, E. & Goebel, B. M.(1994). Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44, 846–849.[CrossRef] [Google Scholar]
  48. Stackebrandt, E., Frederiksen, W., Garrity, G. M. & 10 other authors(2002). Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52, 1043–1047.[CrossRef] [Google Scholar]
  49. Swenson, J. M., Wallace, R. J., Jr, Silcox, V. A. & Thornsberry, C.(1985). Antimicrobial susceptibility of five subgroups of Mycobacterium fortuitum and Mycobacterium chelonae. Antimicrob Agents Chemother 28, 807–811.[CrossRef] [Google Scholar]
  50. Takewaki, S. I., Okuzumi, K., Manabe, I., Tanimura, M., Miyamura, K., Nakahara, K. I., Yazaki, Y., Ohkubo, A. & Nagai, R.(1994). Nucleotide sequence comparison of the mycobacterial dnaJ gene and PCR-restriction fragment length polymorphism analysis for identification of mycobacterial species. Int J Syst Bacteriol 44, 159–166.[CrossRef] [Google Scholar]
  51. Telenti, A., Marchesi, F., Balz, M., Bally, F., Böttger, E. & Bodmer, T.(1993). Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis. J Clin Microbiol 31, 175–178. [Google Scholar]
  52. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G.(1997). The clustal_ x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef] [Google Scholar]
  53. Tiwari, T. S., Ray, B., Jost, K. C. Jr, Rathod, M. K., Zhang, Y., Brown-Elliott, B. A., Hendricks, K. & Wallace, R. J., Jr(2003). Forty years of disinfectant failure: outbreak of postinjection Mycobacterium abscessus infection caused by contamination of benzalkonium chloride. Clin Infect Dis 36, 954–962.[CrossRef] [Google Scholar]
  54. Tortoli, E.(2003). Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s. Clin Microbiol Rev 16, 319–354.[CrossRef] [Google Scholar]
  55. Tortoli, E., Bartoloni, A., Böttger, E. C. & 8 other authors(2001). Burden of unidentifiable mycobacteria in a reference laboratory. J Clin Microbiol 39, 4058–4065.[CrossRef] [Google Scholar]
  56. Turenne, C. Y., Tschetter, L., Wolfe, J. & Kabani, A.(2001). Necessity of quality-controlled 16S rRNA gene sequence databases: identifying nontuberculous Mycobacterium species. J Clin Microbiol 39, 3637–3648.[CrossRef] [Google Scholar]
  57. Vincent, V., Brown-Elliot, B. A., Jost, K. C., Jr & Wallace, R. J., Jr(2003).Mycobacterium: phenotypic and genotypic identification. In Manual of Clinical Microbiology, 8th edn, pp. 560–584. Edited by P. M. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller & R. H. Yolken. Washington, DC: American Society for Microbiology.
  58. Wallace, R. J., Jr, Bedsole, G., Sumter, G., Sanders, C. V., Steele, L. C., Brown, B. A., Smith, J. & Graham, D. R.(1990). Activities of ciprofloxacin and ofloxacin against rapidly growing mycobacteria with demonstration of acquired resistance following single-drug therapy. Antimicrob Agents Chemother 34, 65–70.[CrossRef] [Google Scholar]
  59. Wallace, R. J., Jr, Brown, B. A. & Onyi, G. O.(1991). Susceptibilities of Mycobacterium fortuitum biovar. fortuitum and the two subgroups of Mycobacterium chelonae to imipenem, cefmetazole, cefoxitin, and amoxicillin-clavulanic acid. Antimicrob Agents Chemother 35, 773–775.[CrossRef] [Google Scholar]
  60. Wallace, R. J., Jr, Silcox, V. A., Tsukamura, M., Brown, B. A., Kilburn, J. O., Butler, W. R. & Onyi, G.(1993). Clinical significance, biochemical features, and susceptibility patterns of sporadic isolates of the Mycobacterium chelonae-like organism. J Clin Microbiol 31, 3231–3239. [Google Scholar]
  61. Wallace, R. J., Jr, Glassroth, J., Griffith, D. E., Olivier, K. N., Cook, J. L. & Gordin, F.(1997). Diagnosis and treatment of disease caused by nontuberculous mycobacteria. Am J Resp Crit Care Med 156, S1–S15.[CrossRef] [Google Scholar]
  62. Wallace, R. J., Jr, Brown, B. A. & Griffith, D. E.(1998). Nosocomial outbreaks/pseudo-outbreaks caused by nontuberculous mycobacteria. Annu Rev Microbiol 52, 453–490.[CrossRef] [Google Scholar]
  63. Wallace, R. J., Jr, Zhang, Y., Wilson, R. W., Mann, L. & Rossmore, H.(2002). Presence of a single genotype of the newly described species Mycobacterium immunogenum in industrial metalworking fluids associated with hypersensitivity pneumonitis. Appl Environ Microbiol 68, 5580–5584.[CrossRef] [Google Scholar]
  64. Weisburg, W. G., Barns, S. M., Pelletier, D. A. & Lane, D. J.(1991). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697–703. [Google Scholar]
  65. Wilson, R. W., Steingrube, V. A., Böttger, E. C. & 11 other authors(2001).Mycobacterium immunogenum sp. nov., a novel species related to Mycobacterium abscessus and associated with clinical disease, pseudo-outbreaks and contaminated metalworking fluids: an international cooperative study on mycobacterial taxonomy. Int J Syst Evol Microbiol 51, 1751–1764.[CrossRef] [Google Scholar]
  66. Winthrop, K. L., Abrams, M., Yakrus, M., Schwartz, I., Ely, J., Gillies, D. & Vugia, D. J.(2002). An outbreak of mycobacterial furunculosis associated with footbaths at a nail salon. N Engl J Med 346, 1366–1371.[CrossRef] [Google Scholar]
  67. Woods, G. L., Bergmann, J. S., Witebsky, F. G., Fahle, G. A., Boulet, B., Plaunt, M., Brown, B. A., Wallace, R. J., Jr & Wanger, A.(2000). Multisite reproducibility of Etest for susceptibility testing of Mycobacterium abscessus, Mycobacterium chelonae, and Mycobacterium fortuitum. J Clin Microbiol 38, 656–661. [Google Scholar]
  68. Yakrus, M. A., Hernandez, S. M., Floyd, M. M., Sikes, D., Butler, W. R. & Metchock, B.(2001). Comparison of methods for identification of Mycobacterium abscessus and M. chelonae isolates. J Clin Microbiol 39, 4103–4110.[CrossRef] [Google Scholar]
  69. Yang, S. C., Hsueh, P. R., Lai, H. C. & 7 other authors(2003). High prevalence of antimicrobial resistance in rapidly growing mycobacteria in Taiwan. Antimicrob Agents Chemother 47, 1958–1962.[CrossRef] [Google Scholar]
  70. Zelazny, A. M., Calhoun, L. B., Li, L., Shea, Y. R. & Fischer, S. H.(2005). Identification of Mycobacterium species by secA1 sequences. J Clin Microbiol 43, 1051–1058.[CrossRef] [Google Scholar]
  71. Zolg, J. W. & Philippi-Schulz, S.(1994). The superoxide dismutase gene, a target for detection and identification of mycobacteria by PCR. J Clin Microbiol 32, 2801–2812. [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.63969-0
Loading
rpoB gene sequence-based characterization of emerging non-tuberculous mycobacteria with descriptions of Mycobacterium bolletii sp. nov., Mycobacterium phocaicum sp. nov. and Mycobacterium aubagnense sp. nov.
Int J Syst Evol Microbiol 56, 133 (2006); https://doi.org/10.1099/ijs.0.63969-0
/content/journal/ijsem/10.1099/ijs.0.63969-0
/content/journal/ijsem/10.1099/ijs.0.63969-0
Loading

Data & Media loading...

Supplements

vol. , part 1, pp. 133 - 143

[PDF](72 KB)

PDF

Most cited Most Cited RSS feed

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