Marked microevolution of a unique Mycobacterium tuberculosis Strain in 17 years of ongoing transmission in a high risk population

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Mehaffy, Carolina ^a,b,e   Guthrie, Jennifer L ^a   Alexander, David C ^c   Stuart, Rebecca ^d   Rea, Elizabeth ^d   Jamieson, Frances B ^a,b  

^a PUBLIC HEALTH ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Saskatchewan Disease Control Laboratory   (Canada)

^d TORONTO PUBLIC HEALTH   (Canada)

^e Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM ISOLATE; FEMALE; GENE DELETION; GENE SEQUENCE; GENOTYPING TECHNIQUE; HIGH RISK POPULATION; HOMELESSNESS; HUMAN; MAJOR CLINICAL STUDY; MALE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; TUBERCULOSIS; URBAN AREA; BACTERIAL GENOME; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; TRANSMISSION;

MYCOBACTERIUM TUBERCULOSIS;

BASE SEQUENCE; CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HUMANS; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; TUBERCULOSIS;

EID: 84912118332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112928     Document Type: Article

References (53)

1. Feske ML, Teeter LD, Musser JM, Graviss EA (2013) Counting the homeless: A previously incalculable tuberculosis risk and its social determinants. Am J Public Health 103: 839-848. doi: 10.2105/AJPH.2012.300973.
2. Haddad MB, Wilson TW, Ijaz K, Marks SM, Moore M (2005) Tuberculosis and homelessness in the United States, 1994-2003. JAMA J Am Med Assoc 293: 2762-2766. doi: 10.1001/jama.293.22.2762.
3. Bamrah S, Yelk Woodruff RS, Powell K, Ghosh S, Kammerer JS, et al. (2013) Tuberculosis among the homeless, United States, 1994-2010. Int J Tuberc Lung Dis Off J Int Union Tuberc Lung Dis 17: 1414-1419. doi: 10.5588/ijtld.13.0270.
4. McAdam JM, Bucher SJ, Brickner PW, Vincent RL, Lascher S (2009) Latent tuberculosis and active tuberculosis disease rates among the homeless, New York, New York, USA, 1992-2006. Emerg Infect Dis 15: 1109-1111. doi: 10.3201/eid1507.080410.
5. Khan K, Rea E, McDermaid C, Stuart R, Chambers C, et al. (2011) Active tuberculosis among homeless persons, Toronto, Ontario, Canada, 1998-2007. Emerg Infect Dis 17: 357-365. doi: 10.3201/eid1703.100833.
6. Adam HJ, Guthrie JL, Bolotin S, Alexander DC, Stuart R, et al. (2010) Genotypic characterization of tuberculosis transmission within Toronto's underhoused population, 1997-2008. Int J Tuberc Lung Dis Off J Int Union Tuberc Lung Dis 14: 1350-1353.
7. Lofy KH, McElroy PD, Lake L, Cowan LS, Diem LA, et al. (2006) Outbreak of tuberculosis in a homeless population involving multiple sites of transmission. Int J Tuberc Lung Dis Off J Int Union Tuberc Lung Dis 10: 683-689.
8. Centers for Disease Control and Prevention (CDC) (2012) Tuberculosis outbreak associated with a homeless shelter-Kane County, Illinois, 2007-2011. MMWR Morb Mortal Wkly Rep 61: 186-189.
9. Centers for Disease Control and Prevention (CDC) (2013) Notes from the Field: Outbreak of Tuberculosis Associated with a Newly Identified Mycobacterium tuberculosis Genotype-New York City, 2010-2013. MMWR Morb Mortal Wkly Rep 62: 904.
10. Alexander DC, Guthrie JL, Pyskir D, Maki A, Kurepina N, et al. (2009) Mycobacterium tuberculosis in Ontario, Canada: Insights from IS6110 restriction fragment length polymorphism and mycobacterial interspersed repetitive-unit-variable-number tandem-repeat genotyping. J Clin Microbiol 47: 2651-2654. doi: 10.1128/JCM.01946-08.
11. Bryant JM, Schürch AC, van Deutekom H, Harris SR, de Beer JL, et al. (2013) Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis 13: 110. doi: 10.1186/1471-2334-13-110.
12. Gardy JL, Johnston JC, Sui SJH, Cook VJ, Shah L, et al. (2011) Whole-Genome Sequencing and Social-Network Analysis of a Tuberculosis Outbreak. N Engl J Med 364: 730-739. doi: 10.1056/NEJMoa1003176.
13. Kato-Maeda M, Ho C, Passarelli B, Banaei N, Grinsdale J, et al. (2013) Use of whole genome sequencing to determine the microevolution of Mycobacterium tuberculosis during an outbreak. PloS One 8: E58235. doi: 10.1371/journal. pone.0058235.
14. Schürch AC, Kremer K, Daviena O, Kiers A, Boeree MJ, et al. (2010) Highresolution typing by integration of genome sequencing data in a large tuberculosis cluster. J Clin Microbiol 48: 3403-3406. doi: 10.1128/JCM.00370-10.
15. Walker TM, Ip CLC, Harrell RH, Evans JT, Kapatai G, et al. (2013) Wholegenome sequencing to delineate Mycobacterium tuberculosis outbreaks: A retrospective observational study. Lancet Infect Dis 13: 137-146. doi: 10.1016/S1473-3099 (12) 70277-3.
16. Török ME, Reuter S, Bryant J, Köser CU, Stinchcombe SV, et al. (2013) Rapid whole-genome sequencing for investigation of a suspected tuberculosis outbreak. J Clin Microbiol 51: 611-614. doi: 10.1128/JCM.02279-12.
17. Roetzer A, Diel R, Kohl TA, Rückert C, Nübel U, et al. (2013) Whole Genome Sequencing versus Traditional Genotyping for Investigation of a Mycobacterium tuberculosis Outbreak: A Longitudinal Molecular Epidemiological Study. PLoS Med 10: E1001387. doi: 10.1371/journal.pmed.1001387.
18. Alexander DC, Guthrie JL, Pyskir D, Maki A, Kurepina N, et al. (2009) Mycobacterium tuberculosis in Ontario, Canada: Insights from IS6110 Restriction Fragment Length Polymorphism and Mycobacterial Interspersed Repetitive-Unit-Variable-Number Tandem-Repeat Genotyping. J Clin Microbiol 47: 2651-2654. doi: 10.1128/JCM.01946-08.
19. Van Soolingen D, Hermans PW, de Haas PE, Soll DR, van Embden JD (1991) Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: Evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J Clin Microbiol 29: 2578-2586.
20. Jamieson FB, Guthrie JL, Neemuchwala A, Lastovetska O, Melano RG, et al. (2014) Profiling of rpoB Mutations and MICs to Rifampicin and Rifabutin in Mycobacterium tuberculosis. J Clin Microbiol. doi: 10.1128/JCM.00691-14.
21. Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, et al. (2006) Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 44: 4498-4510. doi: 10.1128/JCM.01392-06.
22. Cowan LS, Diem L, Brake MC, Crawford JT (2004) Transfer of a Mycobacterium tuberculosis genotyping method, Spoligotyping, from a reverse line-blot hybridization, membrane-based assay to the Luminex multianalyte profiling system. J Clin Microbiol 42: 474-477.
23. Van Embden JD, Cave MD, Crawford JT, Dale JW, Eisenach KD, et al. (1993) Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: Recommendations for a standardized methodology. J Clin Microbiol 31: 406-409.
24. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267. doi: 10.1093/molbev/msj030.
25. Gascuel O (1997) BIONJ: An improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14: 685-695.
26. Dress AWM, Huson DH (2004) Constructing splits graphs. IEEEACM Trans Comput Biol Bioinforma IEEE ACM 1: 109-115. doi: 10.1109/TCBB.2004.27.
27. Gambette P, Huson DH (2008) Improved layout of phylogenetic networks. IEEEACM Trans Comput Biol Bioinforma IEEE ACM 5: 472-479. doi: 10.1109/tcbb.2007.1046.
28. Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Systems: 1695.
29. Sampson SL, Richardson M, Van Helden PD, Warren RM (2004) IS6110-mediated deletion polymorphism in isogenic strains of Mycobacterium tuberculosis. J Clin Microbiol 42: 895-898.
30. Chen P, Ruiz RE, Li Q, Silver RF, Bishai WR (2000) Construction and characterization of a Mycobacterium tuberculosis mutant lacking the alternate sigma factor gene, sigF. Infect Immun 68: 5575-5580.
31. Geiman DE, Kaushal D, Ko C, Tyagi S, Manabe YC, et al. (2004) Attenuation of late-stage disease in mice infected by the Mycobacterium tuberculosis mutant lacking the SigF alternate sigma factor and identification of SigF-dependent genes by microarray analysis. Infect Immun 72: 1733-1745.
32. Parida BK, Douglas T, Nino C, Dhandayuthapani S (2005) Interactions of antisigma factor antagonists of Mycobacterium tuberculosis in the yeast two-hybrid system. Tuberculosis 85: 347-355. doi: 10.1016/j.tube.2005.08.001.
33. Hartkoorn RC, Sala C, Uplekar S, Busso P, Rougemont J, et al. (2012) Genome-Wide Definition of the SigF Regulon in Mycobacterium tuberculosis. J Bacteriol 194: 2001-2009. doi: 10.1128/JB.06692-11.
34. Pesavento C, Hengge R (2009) Bacterial nucleotide-based second messengers. Curr Opin Microbiol 12: 170-176. doi: 10.1016/j.mib.2009.01.007.
35. Klinkenberg LG, Lee J, Bishai WR, Karakousis PC (2010) The Stringent Response Is Required for Full Virulence of Mycobacterium tuberculosis in Guinea Pigs. J Infect Dis 202: 1397-1404. doi: 10.1086/656524.
36. Primm TP, Andersen SJ, Mizrahi V, Avarbock D, Rubin H, et al. (2000) The stringent response of Mycobacterium tuberculosis is required for long-Term survival. J Bacteriol 182: 4889-4898.
37. Fang Z, Doig C, Kenna DT, Smittipat N, Palittapongarnpim P, et al. (1999) IS6110-mediated deletions of wild-Type chromosomes of Mycobacterium tuberculosis. J Bacteriol 181: 1014-1020.
38. Ho TB, Robertson BD, Taylor GM, Shaw RJ, Young DB (2000) Comparison of Mycobacterium tuberculosis genomes reveals frequent deletions in a 20 kb variable region in clinical isolates. Yeast Chichester Engl 17: 272-282. doi: 10.1002/1097-0061 (200012) 17: 4,272: : AID-YEA48.3.0.CO; 2-2.
39. Pepperell CS, Casto AM, Kitchen A, Granka JM, Cornejo OE, et al. (2013) The Role of Selection in Shaping Diversity of Natural M. Tuberculosis Populations. PLoS Pathog 9: E1003543. doi: 10.1371/journal.ppat.1003543.
40. Newton SM, Smith RJ, Wilkinson KA, Nicol MP, Garton NJ, et al. (2006) A deletion defining a common Asian lineage of Mycobacterium tuberculosis associates with immune subversion. Proc Natl Acad Sci 103: 15594-15598. doi: 10.1073/pnas.0604283103.
41. Yesilkaya H, Dale JW, Strachan NJC, Forbes KJ (2005) Natural transposon mutagenesis of clinical isolates of Mycobacterium tuberculosis: How many genes does a pathogen need? J Bacteriol 187: 6726-6732. doi: 10.1128/JB.187.19.6726-6732.2005.
42. Reyes A, Sandoval A, Cubillos-Ruiz A, Varley KE, Hernández-Neuta I, et al. (2012) IS-seq: A novel high throughput survey of in vivo IS6110 transposition in multiple Mycobacterium tuberculosis genomes. BMC Genomics 13: 249. doi: 10.1186/1471-2164-13-249.
43. Benedetti A, Menzies D, Behr MA, Schwartzman K, Jin Y (2010) How close is close enough? Exploring matching criteria in the estimation of recent transmission of tuberculosis. Am J Epidemiol 172: 318-326. doi: 10.1093/aje/kwq124.
44. De Boer AS, Kremer K, Borgdorff MW, de Haas PE, Heersma HF, et al. (2000) Genetic heterogeneity in Mycobacterium tuberculosis isolates reflected in IS6110 restriction fragment length polymorphism patterns as low-intensity bands. J Clin Microbiol 38: 4478-4484.
45. Glynn JR, Vynnycky E, Fine PE (1999) Influence of sampling on estimates of clustering and recent transmission of Mycobacterium tuberculosis derived from DNA fingerprinting techniques. Am J Epidemiol 149: 366-371.
46. Schürch AC, Kremer K, Hendriks ACA, Freyee B, McEvoy CRE, et al. (2011) SNP/RD typing of Mycobacterium tuberculosis Beijing strains reveals local and worldwide disseminated clonal complexes. PloS One 6: E28365. doi: 10.1371/journal.pone.0028365.
47. Ford C, Yusim K, Ioerger T, Feng S, Chase M, et al. (2012) Mycobacterium tuberculosis-Heterogeneity revealed through whole genome sequencing. Tuberculosis 92: 194-201. doi: 10.1016/j.tube.2011.11.003.
48. Colangeli R, Arcus VL, Cursons RT, Ruthe A, Karalus N, et al. (2014) Whole Genome Sequencing of Mycobacterium tuberculosis Reveals Slow Growth and Low Mutation Rates during Latent Infections in Humans. PLoS ONE 9: E91024. doi: 10.1371/journal.pone.0091024.
49. Tsolaki AG, Hirsh AE, DeRiemer K, Enciso JA, Wong MZ, et al. (2004) Functional and evolutionary genomics of Mycobacterium tuberculosis: Insights from genomic deletions in 100 strains. Proc Natl Acad Sci 101: 4865-4870. doi: 10.1073/pnas.0305634101.
50. Kruh NA, Troudt J, Izzo A, Prenni J, Dobos KM (2010) Portrait of a Pathogen: The Mycobacterium tuberculosis Proteome In Vivo. PLoS ONE 5: E13938. doi: 10.1371/journal.pone.0013938.
51. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43: 717-731.
52. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, et al. (2006) The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol 60: 312-330. doi: 10.1111/j.1365-2958.2006.05102.x.
53. Arnvig KB, Comas I, Thomson NR, Houghton J, Boshoff HI, et al. (2011) Sequence-Based Analysis Uncovers an Abundance of Non-Coding RNA in the Total Transcriptome of Mycobacterium tuberculosis. PLoS Pathog 7: E1002342. doi: 10.1371/journal.ppat.1002342.