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A New Evolutionary Scenario for the Mycobacterium Tuberculosis Complex

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A New Evolutionary Scenario for the Mycobacterium Tuberculosis Complex A new evolutionary scenario for the Mycobacterium tuberculosis complex R. Brosch*, S. V. Gordon†, M. Marmiesse*, P. Brodin*, C. Buchrieser‡, K. Eiglmeier*, T. Garnier*, C. Gutierrez§, G. Hewinson†, K. Kremer¶, L. M. Parsonsʈ, A. S. Pym*, S. Samper**, D. van Soolingen¶, and S. T. Cole*†† *Unite´deGe´ne´ tique Mole´culaire Bacte´rienne, ‡Laboratoire de Ge´nomique des Microorganismes Pathoge`nes, and §Centre National de Re´fe´ rence des Mycobacte´ries, Institut Pasteur, 25-28 Rue du Docteur Roux, 75724 Paris Cedex 15, France; †Veterinary Laboratories Agency, Woodham Lane, New Haw, Addlestone, Surrey KT15 3NB, United Kingdom; ¶Mycobacteria Reference Department, Diagnostic Laboratory for Infectious Diseases and Perinatal Screening, National Institute of Public Health and the Environment, 3720 BA Bilthoven, The Netherlands; ʈWadsworth Center, New York State Department of Health and School of Public Health, State University of New York at Albany, David Axelrod Institute, Albany, NY 12201-2002; and **Departamento de Microbiologia, Medicina Preventiva y Salud Publica, Universidad de Zaragoza, C͞Domingo Miralsn, 50009 Zaragoza, Spain Edited by John Maynard Smith, University of Sussex, Brighton, United Kingdom, and approved January 9, 2002 (received for review October 15, 2001) The distribution of 20 variable regions resulting from insertion- roughly 15,000–20,000 years ago (2). Also, it has been speculated deletion events in the genomes of the tubercle bacilli has been that M. tuberculosis, the most widespread etiological agent of evaluated in a total of 100 strains of Mycobacterium tuberculosis, human tuberculosis has evolved from M. bovis, the agent of Mycobacterium africanum, Mycobacterium canettii, Mycobacte- bovine tuberculosis, by specific adaptation of an animal patho- rium microti, and Mycobacterium bovis. This approach showed that gen to the human host (3). However, both hypotheses were the majority of these polymorphisms did not occur independently proposed before the whole genome sequence of M. tuberculosis in the different strains of the M. tuberculosis complex but, rather, (4) was available and before comparative genomics uncovered resulted from ancient, irreversible genetic events in common several variable genomic regions in the members of the M. progenitor strains. Based on the presence or absence of an M. tuberculosis complex. Differential hybridization arrays identified tuberculosis specific deletion (TbD1), M. tuberculosis strains can be 14 regions of difference (RD1–14), ranging in size from 2 to 12.7 divided into ancestral and ‘‘modern’’ strains, the latter comprising kb, that were absent from bacillus Calmette–Gue´rin Pasteur representatives of major epidemics like the Beijing, Haarlem, and relative to M. tuberculosis H37Rv (5, 6). In parallel, six regions, African M. tuberculosis clusters. Furthermore, successive loss of H37Rv related deletions (RvD)1–5, and M. tuberculosis specific DNA, reflected by region of difference 9 and other subsequent deletion 1 (TbD1), that were absent from the M. tuberculosis deletions, was identified for an evolutionary lineage represented H37Rv genome relative to other members of the M. tuberculosis by M. africanum, M. microti, and M. bovis that diverged from the complex were revealed by comparative genomics approaches progenitor of the present M. tuberculosis strains before TbD1 employing pulsed-field gel electrophoresis techniques (5, 7) and occurred. These findings contradict the often-presented hypothe- in silico comparisons of the near complete M. bovis AF2122͞97 sis that M. tuberculosis, the etiological agent of human tubercu- genome sequence and the M. tuberculosis H37Rv sequence. losis evolved from M. bovis, the agent of bovine disease. M. canettii In the present study, we have analyzed the distribution of these and ancestral M. tuberculosis strains lack none of these deleted 20 variable regions situated around the genome (see Table 1, regions, and, therefore, seem to be direct descendants of tubercle which is published as supporting information on the PNAS web bacilli that existed before the M. africanum3M. bovis lineage site, www.pnas.org) in a representative and diverse set of 100 separated from the M. tuberculosis lineage. This observation sug- strains belonging to the M. tuberculosis complex. The strains were gests that the common ancestor of the tubercle bacilli resembled isolated from different hosts and from a broad range of geo- M. tuberculosis or M. canettii and could well have been a human graphic origins, and exhibit a wide spectrum of typing charac- pathogen already. teristics like IS6110 and spoligotype hybridization patterns or variable-number tandem repeats of mycobacterial interspersed evolution ͉ diagnostic ͉ identification repetitive units (MIRU-VNTR; refs. 8 and 9). We have found striking evidence that deletion of certain variable genomic he mycobacteria grouped in the Mycobacterium tuberculosis regions did not occur independently in the different strains of the Tcomplex are characterized by 99.9% similarity at the nucle- M. tuberculosis complex; assuming that there is little or no otide level and identical 16S rRNA sequences (1, 2) but differ recombination of chromosomal segments between the various widely in terms of their host tropisms, phenotypes, and patho- lineages of the complex, this allows us to propose a completely genicity. Assuming that they all are derived from a common new scenario for the evolution of the M. tuberculosis complex and ancestor, it is intriguing that some are exclusively human (M. the origin of human tuberculosis. tuberculosis, Mycobacterium africanum, Mycobacterium canettii) or rodent pathogens (Mycobacterium microti), whereas others Material and Methods have a wide host spectrum (Mycobacterium bovis). What was the Bacterial Strains. The 100 M. tuberculosis complex strains were genetic organization of the last common ancestor of the tubercle composed of 46 M. tuberculosis strains isolated in 30 countries, bacilli, and in which host did it live? Which genetic events may have contributed to the fact that the host spectrum is so different and often specific? Where and when did M. tuberculosis evolve? This paper was submitted directly (Track II) to the PNAS office. Answers to these questions are important for a better under- Abbreviations: TbD1, M. tuberculosis specific deletion 1; RvD, H37Rv related deletion; RD, standing of the pathogenicity and the global epidemiology of region of difference. tuberculosis and may help to anticipate future trends in the Data deposition: The sequences reported in this paper have been deposited in the EMBL database (accession nos. AJ426486, AJ003103, AJ007301, AJ131210, Y18604, and spread of the disease. AJ132559). Because of the unusually high degree of conservation in their ††To whom reprint requests should be addressed. E-mail: [email protected]. housekeeping genes, it has been suggested that the members of The publication costs of this article were defrayed in part by page charge payment. This the M. tuberculosis complex underwent an evolutionary bottle- article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. neck at the time of speciation, estimated to have occurred §1734 solely to indicate this fact. 3684–3689 ͉ PNAS ͉ March 19, 2002 ͉ vol. 99 ͉ no. 6 www.pnas.org͞cgi͞doi͞10.1073͞pnas.052548299 Downloaded by guest on October 1, 2021 14 M. africanum strains, 28 M. bovis strains originating in 5 RD9, and RD10 in bacillus Calmette–Gue´rin were deposited in countries, 2 M. bovis bacillus Calmette–Gue´rin vaccine strains the EMBL database under accession nos. AJ003103, AJ007301, (Pasteur and Japan), 5 M. microti strains, and 5 M. canettii strains. AJ131210, Y18604, and AJ132559, respectively. The strains were isolated from human and animal sources and were selected to represent a wide diversity, including 60 strains Results that have been used in a multicenter study (8). The M. africanum Variable Genomic Regions and Their Occurrence in the Members of the strains were retrieved from the collection of the Wadsworth M. tuberculosis Complex. The PCR screening assay for the 20 Center (New York State Department of Health, Albany, NY), variable regions (Table 1) within 46 M. tuberculosis,14M. whereas the majority of the M. bovis isolates came from the africanum,5M. canettii,5M. microti, 28 M. bovis, and 2 bacillus collection of the University of Zaragoza (Zaragoza, Spain). Four Calmette–Gue´rin strains used oligonucleotides internal to M. canettii strains are from the culture collection of the Pasteur known RDs and RvDs, as well as oligonucleotides flanking these Institute (Paris, France). The strains have been extensively regions (Table 1). This approach generated a large data set that characterized by reference typing methods, i.e., IS6110 restric- was robust, highly reliable, and internally controlled, because tion fragment length polymorphism (RFLP) typing and spoli- PCR amplicons obtained with the internal primer pair corre- gotyping. M. tuberculosis H37Rv, M. tuberculosis H37Ra, M. lated with the absence of an appropriately sized amplicon with ͞ tuberculosis CDC1551, M. bovis AF2122 97, M. microti OV254, the flanking primer-pair, and vice versa. and M. canettii CIPT 140010059 were included as reference According to the conservation of junction sequences flanking strains. DNA was prepared as described (10). the variable regions, three types of regions were distinguished, each one having a different importance as an evolutionary Genome Comparisons and Primer Design. For
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