Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 20, Number 3—March 2014

High-level Relatedness among Mycobacterium abscessus subsp. massiliense Strains from Widely Separated Outbreaks

Hervé Tettelin, Rebecca M. Davidson, Sonia Agrawal, Moira L. Aitken, Shamira Shallom, Nabeeh A. Hasan, Michael Strong, Vinicius Calado Nogueira de Moura, Mary Ann De Groote, Rafael S. Duarte, Erin Hine, Sushma Parankush, Qi Su, Sean C. Daugherty, Claire M. Fraser, Barbara A. Brown-Elliott, Richard J. Wallace, Steven M. Holland, Elizabeth P. Sampaio, Kenneth N. Olivier, Mary Jackson, and Adrian M. ZelaznyComments to Author 
Author affiliations: University of Maryland School of Medicine, Baltimore, Maryland, USA (H. Tettelin, S. Agrawal, E. Hine, S. Parankush, Q. Su, S.C. Daugherty, C.M. Fraser); National Jewish Health, Denver, Colorado, USA (R.M. Davidson, N.A. Hasan, M. Strong); University of Washington, Seattle, Washington, USA (M.L. Aitken); National Institutes of Health, Bethesda, Maryland, USA (S. Shallom, S.M. Holland, E.P. Sampaio, K.N. Olivier, A.M. Zelazny); University of Colorado Denver, Aurora, Colorado, USA (N.A. Hasan, M. Strong); Colorado State University, Fort Collins, Colorado, USA (V. Calado Nogueira de Moura, M.A. De Groote, M. Jackson); Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (R.S. Duarte); University of Texas Health Northeast, Tyler, Texas, USA (B.A. Brown-Elliott, R.J. Wallace Jr.)

Main Article

Figure 1

Neighbor-joining phylogenetic tree based on whole-genome multiple alignment of 24 Mycobacterium abscessus group genomes. Genomes in Table 1 were aligned by using Mugsy (22), core segments of the alignment were identified by using Phylomark (23), and resulting concatenated nucleotide sequences were used for construction of the midpoint-rooted neighbor-joining phylogenetic tree by using MEGA (24). Strains from an outbreak of M. abscessus subsp. massiliense infections at a cystic fibrosis center in

Figure 1. Neighbor-joining phylogenetic tree based on whole-genome multiple alignment of 24 Mycobacterium abscessus group genomesGenomes in Table 1 were aligned by using Mugsy (22), core segments of the alignment were identified by using Phylomark (23), and resulting concatenated nucleotide sequences were used for construction of the midpoint-rooted neighbor-joining phylogenetic tree by using MEGA (24)Strains from an outbreak of Mabscessus subspmassiliense infections at a cystic fibrosis center in Seattle, Washington, USA, are indicated in red; strains from an outbreak of Mabscessus subspmassiliense infections at a cystic fibrosis center in Papworth, UK, are indicated in blue (cluster 1) and purple (cluster 2); strains from Brazil are indicated in magenta; and the Mabscessus subspmassiliense type strain is indicated in greenBoostrap values obtained after 100 iterations were ≥97 for all nodes of the tree except 70 for the node separating strain M115 from the outbreak cluster and 40 and 41 for 2 nodes within the Papworth cluster 1 (6)SNPs, single-nucleotide polymorphisms.

Main Article

  1. Levy  I, Grisaru-Soen  G, Lerner-Geva  L, Kerem  E, Blau  H, Bentur  L, Multicenter cross-sectional study of nontuberculous mycobacterial infections among cystic fibrosis patients, Israel. Emerg Infect Dis. 2008;14:37884 . DOIPubMed
  2. Olivier  KN, Weber  DJ, Wallace  RJ Jr, Faiz  AR, Lee  JH, Zhang  Y, Nontuberculous mycobacteria. I: multicenter prevalence study in cystic fibrosis. Am J Respir Crit Care Med. 2003;167:82834. DOIPubMed
  3. Roux  AL, Catherinot  E, Ripoll  F, Soismier  N, Macheras  E, Ravilly  S, Multicenter study of prevalence of nontuberculous mycobacteria in patients with cystic fibrosis in France. J Clin Microbiol. 2009;47:41248. DOIPubMed
  4. Sermet-Gaudelus  I, Le Bourgeois  M, Pierre-Audigier  C, Offredo  C, Guillemot  D, Halley  S, Mycobacterium abscessus and children with cystic fibrosis. Emerg Infect Dis. 2003;9:158791. DOIPubMed
  5. Aitken  ML, Limaye  A, Pottinger  P, Whimbey  E, Goss  CH, Tonelli  MR, Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med. 2012;185:2312. DOIPubMed
  6. Bryant  JM, Grogono  DM, Greaves  D, Foweraker  J, Roddick  I, Inns  T, Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet. 2013;381:155160 . DOIPubMed
  7. Davidson  RM, Reynolds  PR, Farias-Hesson  E, Duarte  RS, Jackson  M, Strong  M. Genome sequence of an epidemic isolate of Mycobacterium abscessus subsp. bolletii from Rio de Janeiro, Brazil. Genome Announc. 2013;1:e00617–13.
  8. Raiol  T, Ribeiro  GM, Maranhao  AQ, Bocca  AL, Silva-Pereira  I, Junqueira-Kipnis  AP, Complete genome sequence of Mycobacterium massiliense. J Bacteriol. 2012;194:5455. DOIPubMed
  9. Chan  J, Halachev  M, Yates  E, Smith  G, Pallen  M. Whole-genome sequence of the emerging pathogen Mycobacterium abscessus strain 47J26. J Bacteriol. 2012;194:549. DOIPubMed
  10. Ngeow  YF, Wong  YL, Tan  JL, Arumugam  R, Wong  GJ, Ong  CS, Genome sequence of Mycobacterium massiliense M18, isolated from a lymph node biopsy specimen. J Bacteriol. 2012;194:4125. DOIPubMed
  11. Ngeow  YF, Wong  YL, Lokanathan  N, Wong  GJ, Ong  CS, Ng  KP, Genomic analysis of Mycobacterium massiliense strain M115, an isolate from human sputum. J Bacteriol. 2012;194:4786 and. DOIPubMed
  12. Ngeow  YF, Wee  WY, Wong  YL, Tan  JL, Ongi  CS, Ng  KP, Genomic analysis of Mycobacterium abscessus strain M139, which has an ambiguous subspecies taxonomic position. J Bacteriol. 2012;194:60023. DOIPubMed
  13. Choo  SW, Wong  YL, Tan  JL, Ong  CS, Wong  GJ, Ng  KP, Annotated genome sequence of Mycobacterium massiliense strain M154, belonging to the recently created taxon Mycobacterium abscessus subsp. bolletii comb. nov. J Bacteriol. 2012;194:4778. DOIPubMed
  14. Kim  BJ, Kim  BR, Hong  SH, Seok  SH, Kook  YH. Complete genome sequence of Mycobacterium massiliense clinical strain Asan 50594, belonging to the type II genotype. Genome Announc. 2013;1:e00429–13.
  15. Tettelin  H, Sampaio  EP, Daugherty  SC, Hine  E, Riley  DR, Sadzewicz  L, Genomic insights into the emerging human pathogen Mycobacterium massiliense. J Bacteriol. 2012;194:5450 . DOIPubMed
  16. Adékambi  T, Reynaud-Gaubert  M, Greub  G, Gevaudan  MJ, La Scola  B, Raoult  D, Amoebal coculture of “Mycobacterium massiliense” sp. nov. from the sputum of a patient with hemoptoic pneumonia. J Clin Microbiol. 2004;42:5493501 . DOIPubMed
  17. Pawlik  A, Garnier  G, Orgeur  M, Tong  P, Lohan  A, Le Chevalier  F, Identification and characterization of the genetic changes responsible for the characteristic smooth-to-rough morphotype alterations of clinically persistent Mycobacterium abscessus. Mol Microbiol. 2013;3:•••; Epub ahead of print and.PubMed
  18. Ripoll  F, Pasek  S, Schenowitz  C, Dossat  C, Barbe  V, Rottman  M, Non mycobacterial virulence genes in the genome of the emerging pathogen Mycobacterium abscessus. PLoS ONE. 2009;4:e5660. DOIPubMed
  19. Choi  GE, Cho  YJ, Koh  WJ, Chun  J, Cho  SN, Shin  SJ. Draft genome sequence of Mycobacterium abscessus subsp. bolletii BD(T). J Bacteriol. 2012;194:27567 . DOIPubMed
  20. Wong  YL, Choo  SW, Tan  JL, Ong  CS, Ng  KP, Ngeow  YF. Draft genome sequence of Mycobacterium bolletii strain M24, a rapidly growing mycobacterium of contentious taxonomic status. J Bacteriol. 2012;194:4475 . DOIPubMed
  21. Zerbino  DR, Birney  E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:8219. DOIPubMed
  22. Angiuoli  SV, Salzberg  SL. Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics. 2011;27:33442. DOIPubMed
  23. Sahl  JW, Matalka  MN, Rasko  DA. Phylomark, a tool to identify conserved phylogenetic markers from whole-genome alignments. Appl Environ Microbiol. 2012;78:488492. DOIPubMed
  24. Tamura  K, Peterson  D, Peterson  N, Stecher  G, Nei  M, Kumar  S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:27319. DOIPubMed
  25. Li  H, Durbin  R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:175460. DOIPubMed
  26. McKenna  A, Hanna  M, Banks  E, Sivachenko  A, Cibulskis  K, Kernytsky  A, The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297303. DOIPubMed
  27. Macheras  E, Roux  AL, Ripoll  F, Sivadon-Tardy  V, Gutierrez  C, Gaillard  JL, Inaccuracy of single-target sequencing for discriminating species of the Mycobacterium abscessus group. J Clin Microbiol. 2009;47:2596600. DOIPubMed
  28. Adékambi  T, Colson  P, Drancourt  M. rpoB-based identification of nonpigmented and late-pigmenting rapidly growing mycobacteria. J Clin Microbiol. 2003;41:5699708. DOIPubMed
  29. Zelazny  AM, Root  JM, Shea  YR, Colombo  RE, Shamputa  IC, Stock  F, Cohort study of molecular identification and typing of Mycobacterium abscessus, Mycobacterium massiliense, and Mycobacterium bolletii. J Clin Microbiol. 2009;47:198595. DOIPubMed
  30. Macheras  E, Roux  AL, Bastian  S, Leao  SC, Palaci  M, Sivadon-Tardy  V, Multilocus sequence analysis and rpoB sequencing of Mycobacterium abscessus (sensu lato) strains. J Clin Microbiol. 2011;49:4919. DOIPubMed
  31. Thompson  JD, Higgins  DG, Gibson  TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:467380. DOIPubMed
  32. Duarte  RS, Lourenco  MC, Fonseca Lde  S, Leao  SC, Amorim Ede  L, Rocha  IL, Epidemic of postsurgical infections caused by Mycobacterium massiliense. J Clin Microbiol. 2009;47:214955. DOIPubMed
  33. Leão  SC, Viana-Niero  C, Matsumoto  CK, Lima  KV, Lopes  ML, Palaci  M, Epidemic of surgical-site infections by a single clone of rapidly growing mycobacteria in Brazil. Future Microbiol. 2010;5:97180. DOIPubMed
  34. Varela  C, Rittmann  D, Singh  A, Krumbach  K, Bhatt  K, Eggeling  L, MmpL genes are associated with mycolic acid metabolism in mycobacteria and corynebacteria. Chem Biol. 2012;19:498506. DOIPubMed
  35. Leão  SC, Matsumoto  CK, Carneiro  A, Ramos  RT, Nogueira  CL, Lima  JD Jr, The detection and sequencing of a broad-host-range conjugative IncP-1beta plasmid in an epidemic strain of Mycobacterium abscessus subsp. bolletii. PLoS ONE. 2013;8:e60746. DOIPubMed
  36. Wallace  RJ Jr, Meier  A, Brown  BA, Zhang  Y, Sander  P, Onyi  GO, Genetic basis for clarithromycin resistance among isolates of Mycobacterium chelonae and Mycobacterium abscessus. Antimicrob Agents Chemother. 1996;40:167681 .PubMed
  37. Prammananan  T, Sander  P, Brown  BA, Frischkorn  K, Onyi  GO, Zhang  Y, A single 16S ribosomal RNA substitution is responsible for resistance to amikacin and other 2-deoxystreptamine aminoglycosides in Mycobacterium abscessus and Mycobacterium chelonae. J Infect Dis. 1998;177:157381. DOIPubMed
  38. Shallom  SJ, Gardina  PJ, Myers  TG, Sebastian  Y, Conville  P, Calhoun  LB, New rapid scheme for distinguishing the subspecies of the Mycobacterium abscessus group and identification of Mycobacterium massiliense with inducible clarithromycin resistance. J Clin Microbiol. 2013;51:29439. DOIPubMed
  39. Koh  WJ, Jeon  K, Lee  NY, Kim  BJ, Kook  YH, Lee  SH, Clinical significance of differentiation of Mycobacterium massiliense from Mycobacterium abscessus. Am J Respir Crit Care Med. 2011;183:40510. DOIPubMed
  40. Bange  FC, Brown  BA, Smaczny  C, Wallace  RJ Jr, Bottger  EC. Lack of transmission of Mycobacterium abscessus among patients with cystic fibrosis attending a single clinic. Clin Infect Dis. 2001;32:164850. DOIPubMed

Main Article

Page created: February 19, 2014
Page updated: February 19, 2014
Page reviewed: February 19, 2014
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.