Home LiteratureArticle Details
PMID: 19881526 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Comparative genomic and phylogeographic analysis of Mycobacterium leprae.

Nature genetics ·Vol. 41 ·No. 12 ·2009-12-00 ·Pages 1282-9

Monot M, Honoré N, Garnier T, Zidane N, Sherafi D, Paniz-Mondolfi A, Matsuoka M, Taylor GM, Donoghue HD, Bouwman A, Mays S, Watson C, Lockwood D, Khamesipour A, Khamispour A, Dowlati Y, Jianping S, Rea TH, Vera-Cabrera L, Stefani MM, Banu S, Macdonald M, Sapkota BR, Spencer JS, Thomas J, Harshman K, Singh P, Busso P, Gattiker A, Rougemont J, Brennan PJ, Cole ST

Abstract

Reductive evolution and massive pseudogene formation have shaped the 3.31-Mb genome of Mycobacterium leprae, an unculturable obligate pathogen that causes leprosy in humans. The complete genome sequence of M. leprae strain Br4923 from Brazil was obtained by conventional methods (6x coverage), and Illumina resequencing technology was used to obtain the sequences of strains Thai53 (38x coverage) and NHDP63 (46x coverage) from Thailand and the United States, respectively. Whole-genome comparisons with the previously sequenced TN strain from India revealed that the four strains share 99.995% sequence identity and differ only in 215 polymorphic sites, mainly SNPs, and by 5 pseudogenes. Sixteen interrelated SNP subtypes were defined by genotyping both extant and extinct strains of M. leprae from around the world. The 16 SNP subtypes showed a strong geographical association that reflects the migration patterns of early humans and trade routes, with the Silk Road linking Europe to China having contributed to the spread of leprosy.

MeSH Terms
Genes, Bacterial Genome, Bacterial Geography Humans Leprosy/genetics,microbiology Mycobacterium leprae/classification,genetics Phylogeny Polymorphism, Single Nucleotide Recombination, Genetic
Authors & Affiliations
32 authors, click to expand affiliations / ORCID
Monot Marc
Institut Pasteur, Paris, France.
Honoré Nadine
Garnier Thierry
Zidane Nora
Sherafi Diana
Paniz-Mondolfi Alberto
Matsuoka Masanori
Taylor G Michael
Donoghue Helen D
Bouwman Abi
Mays Simon
Watson Claire
Lockwood Diana
Khamesipour Ali
Khamispour Ali
Dowlati Yahya
Jianping Shen
Rea Thomas H
Vera-Cabrera Lucio
Stefani Mariane M
Banu Sayera
Macdonald Murdo
Sapkota Bishwa Raj
Spencer John S
Thomas Jérôme
Harshman Keith
Singh Pushpendra
Busso Philippe
Gattiker Alexandre
Rougemont Jacques
Brennan Patrick J
Cole Stewart T
References (57)
57 references, click to expand
  1. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens.
    Annu Rev Microbiol. 2008;62:53-70 PMID: 18785837
  2. The complete genome sequence of Mycobacterium bovis.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7877-82 PMID: 12788972
  3. Sequence type analysis and recombinational tests (START).
    Bioinformatics. 2001 Dec;17(12):1230-1 PMID: 11751234
  4. Are variable-number tandem repeats appropriate for genotyping Mycobacterium leprae?
    J Clin Microbiol. 2008 Jul;46(7):2291-7 PMID: 18495858
  5. Massive gene decay in the leprosy bacillus.
    Nature. 2001 Feb 22;409(6823):1007-11 PMID: 11234002
  6. Diversity of potential short tandem repeats in Mycobacterium leprae and application for molecular typing.
    J Clin Microbiol. 2005 Oct;43(10):5221-9 PMID: 16207987
  7. ACT: the Artemis Comparison Tool.
    Bioinformatics. 2005 Aug 15;21(16):3422-3 PMID: 15976072
  8. Mapping short DNA sequencing reads and calling variants using mapping quality scores.
    Genome Res. 2008 Nov;18(11):1851-8 PMID: 18714091
  9. Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis.
    Emerg Infect Dis. 2004 Sep;10(9):1568-77 PMID: 15498158
  10. Genes required for mycobacterial growth defined by high density mutagenesis.
    Mol Microbiol. 2003 Apr;48(1):77-84 PMID: 12657046
  11. A rapid bootstrap algorithm for the RAxML Web servers.
    Syst Biol. 2008 Oct;57(5):758-71 PMID: 18853362
  12. Traces of human migrations in Helicobacter pylori populations.
    Science. 2003 Mar 7;299(5612):1582-5 PMID: 12624269
  13. Multiple polymorphic loci for molecular typing of strains of Mycobacterium leprae.
    J Clin Microbiol. 2004 Apr;42(4):1666-72 PMID: 15071023
  14. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis.
    Genome Res. 2008 May;18(5):729-41 PMID: 18403782
  15. Leprosy.
    Lancet. 2004 Apr 10;363(9416):1209-19 PMID: 15081655
  16. Repetitive sequences in Mycobacterium leprae and their impact on genome plasticity.
    Lepr Rev. 2001 Dec;72(4):449-61 PMID: 11826481
  17. Technical note: improved DNA extraction from ancient bones using silica-based spin columns.
    Am J Phys Anthropol. 1998 Apr;105(4):539-43 PMID: 9584894
  18. On the origin of leprosy.
    Science. 2005 May 13;308(5724):1040-2 PMID: 15894530
  19. A rapid method for the detection of potentially viable Mycobacterium leprae in human biopsies: a novel application of PCR.
    FEMS Microbiol Lett. 1989 Dec;53(3):305-9 PMID: 2693204
  20. A new DNA sequence assembly program.
    Nucleic Acids Res. 1995 Dec 25;23(24):4992-9 PMID: 8559656
  21. Reconstructing the ancestor of Mycobacterium leprae: the dynamics of gene loss and genome reduction.
    Genome Res. 2007 Aug;17(8):1178-85 PMID: 17623808
  22. Variable numbers of TTC repeats in Mycobacterium leprae DNA from leprosy patients and use in strain differentiation.
    J Clin Microbiol. 2000 Dec;38(12):4535-8 PMID: 11101592
  23. Did the loss of sigma factors initiate pseudogene accumulation in M. leprae?
    Trends Microbiol. 2003 Feb;11(2):59-61 PMID: 12598124
  24. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  25. The Mycobacterium tuberculosis Rv2358-furB operon is induced by zinc.
    Res Microbiol. 2004 Apr;155(3):192-200 PMID: 15059632
  26. De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer.
    Genome Res. 2008 May;18(5):802-9 PMID: 18332092
  27. Aquatic insects as a vector for Mycobacterium ulcerans.
    Appl Environ Microbiol. 2002 Sep;68(9):4623-8 PMID: 12200321
  28. Inferring the pattern of spontaneous mutation from the pattern of substitution in unitary pseudogenes of Mycobacterium leprae and a comparison of mutation patterns among distantly related organisms.
    J Mol Evol. 2005 Dec;61(6):795-803 PMID: 16315108
  29. A family of dispersed repeats in Mycobacterium leprae.
    Mol Microbiol. 1990 Oct;4(10):1745-51 PMID: 2077358
  30. A reappraisal of early hominid phylogeny.
    J Hum Evol. 1997 Jan;32(1):17-82 PMID: 9034954
  31. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  32. Comparisons of dN/dS are time dependent for closely related bacterial genomes.
    J Theor Biol. 2006 Mar 21;239(2):226-35 PMID: 16239014
  33. Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon.
    J Bacteriol. 2007 Feb;189(3):730-40 PMID: 17098899
  34. Identification and distribution of Mycobacterium leprae genotypes in a region of high leprosy prevalence in China: a 3-year molecular epidemiological study.
    J Clin Microbiol. 2007 Jun;45(6):1728-34 PMID: 17428944
  35. Mycobacterium ulcerans in mosquitoes captured during outbreak of Buruli ulcer, southeastern Australia.
    Emerg Infect Dis. 2007 Nov;13(11):1653-60 PMID: 18217547
  36. Genotypic variation and stability of four variable-number tandem repeats and their suitability for discriminating strains of Mycobacterium leprae.
    J Clin Microbiol. 2004 Jun;42(6):2558-65 PMID: 15184434
  37. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi.
    Nat Genet. 2008 Aug;40(8):987-93 PMID: 18660809
  38. Genome sequence of Yersinia pestis, the causative agent of plague.
    Nature. 2001 Oct 4;413(6855):523-7 PMID: 11586360
  39. Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh.
    Proc Natl Acad Sci U S A. 2004 Apr 6;101(14):4746-51 PMID: 15051885
  40. Global leprosy situation, 2007.
    Wkly Epidemiol Rec. 2007 Jun 22;82(25):225-32 PMID: 17585406
  41. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer.
    Genome Res. 2007 Feb;17(2):192-200 PMID: 17210928
  42. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  43. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.
    Bioinformatics. 2006 Nov 1;22(21):2688-90 PMID: 16928733
  44. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica.
    Nat Genet. 2003 Sep;35(1):32-40 PMID: 12910271
  45. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography.
    PLoS Biol. 2008 Dec 16;6(12):e311 PMID: 19090620
  46. Rv2358 and FurB: two transcriptional regulators from Mycobacterium tuberculosis which respond to zinc.
    J Bacteriol. 2005 Aug;187(16):5837-40 PMID: 16077132
  47. Microevolution and history of the plague bacillus, Yersinia pestis.
    Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17837-42 PMID: 15598742
  48. The application of molecular genetic approaches to the study of human evolution.
    Nat Genet. 2003 Mar;33 Suppl:266-75 PMID: 12610536
  49. Y chromosome sequence variation and the history of human populations.
    Nat Genet. 2000 Nov;26(3):358-61 PMID: 11062480
  50. Artemis: sequence visualization and annotation.
    Bioinformatics. 2000 Oct;16(10):944-5 PMID: 11120685
  51. Microsatellite mapping of Mycobacterium leprae populations in infected humans.
    J Clin Microbiol. 2004 Nov;42(11):4931-6 PMID: 15528676
  52. APE: Analyses of Phylogenetics and Evolution in R language.
    Bioinformatics. 2004 Jan 22;20(2):289-90 PMID: 14734327
  53. Use of short tandem repeat sequences to study Mycobacterium leprae in leprosy patients in Malawi and India.
    PLoS Negl Trop Dis. 2008 Apr 09;2(4):e214 PMID: 18398487
  54. 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 Nov 11;22(22):4673-80 PMID: 7984417
  55. Variable host-pathogen compatibility in Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2869-73 PMID: 16477032
  56. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  57. An African origin for the intimate association between humans and Helicobacter pylori.
    Nature. 2007 Feb 22;445(7130):915-918 PMID: 17287725
Article Info
Journal
Nature genetics
Abbr.
Nat Genet
ISSN
1546-1718
Published
2009-12-00
Epub
2009-00-01
Pages
1282-9
Language
English
Region
United States
NLM ID
9216904
Subset
IM
Grants
NIAID NIH HHS · N01-AI25469 · United States
NIAID NIH HHS · R01-AI47197-01A1 · United States
Corrections
ErratumIn
-
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]