MBE Advance Access originally published online on March 6, 2006
Molecular Biology and Evolution 2006 23(6):1129-1135; doi:10.1093/molbev/msj120
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Research Article |
Horizontal Transfer of a Virulence Operon to the Ancestor of Mycobacterium tuberculosis
* Unit of Mycobacterial Genetics, Institut Pasteur, Paris, France; Molecular and Genomics Bioinformatics, Institut National de la Santé et de la Recherche Médicale 726, University Paris 7, Paris, France; Centre National de la Recherche Scientifique Formation de Recherche en Evolution 2849, Institut Pasteur, Paris, France; Unit of Bacterial Molecular Genetics, Institut Pasteur, Paris, France; and || Centre National de la Recherche Scientifique Unité de Recherche Associée 2172, Institut Pasteur, Paris, France
E-mail: neyrolle{at}pasteur.fr.
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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The contribution of interspecies horizontal gene transfer (HGT) to the evolution and virulence of Mycobacterium tuberculosis, the agent of tuberculosis in humans, has been barely investigated. Here we have studied the evolutionary history of the M. tuberculosis Rv0986-8 virulence operon recently identified, through functional genomics approaches, as playing an important role in parasitism of host phagocytic cells. We showed that among actinobacteria, this operon is specific to the M. tuberculosis complex and to ancestral Mycobacterium prototuberculosis species. These data, together with phylogenetic reconstruction and other in silico analyses, provided strong evidence that this operon has been aquired horizontally by the ancestor of M. tuberculosis, before the recent evolutionary bottleneck that preceded the clonal-like evolution of the M. tuberculosis complex. Genomic signature profiling further suggested that the transfer was plasmid mediated and that the operon originated from a
-proteobacterium donor species. Our study points out for the first time the contribution of HGT to the emergence of M. tuberculosis and close relatives as major pathogens. In addition, our data underline the importance of deciphering gene transfer networks in M. tuberculosis in order to better understand the evolutionary mechanisms involved in mycobacterial virulence.
Key Words: horizontal gene transfer • Mycobacterium tuberculosis • tuberculosis • virulence
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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Horizontal gene transfer (HGT) between unrelated species is thought to be an additional factor driving genetic diversity, especially in bacteria (Ochman, Lawrence, and Groisman 2000
; Boucher et al. 2003; Jain et al. 2003; Philippe and Douady 2003). HGT provides the host organism with new genes that under certain selective pressures may prove to confer a selective advantage and therefore may be maintained and/or expanded within the population. In a number of pathogenic bacteria, several virulence genes and gene clusters, called pathogenicity islands, have been acquired by HGT (Ochman, Lawrence, and Groisman 2000). This mechanism does not seem to be common in mycobacteria, in which a limited number of genes are proposed to have been acquired through HGT (Martin et al. 1990; Blanc-Potard and Lafay 2003; Kinsella et al. 2003). In all cases, these few genes are observed in fast- and slow-growing mycobacteria species, indicating that they likely represent ancient episodes of HGT occurred in an ancestor of the whole Mycobacterium genus. The apparent paucity of horizontally transferred genes in mycobacterial chromosomes is supported by recent genetic and genomic studies. For instance, whole-genome analysis of the chromosomes of Mycobacterium tuberculosis and of Mycobacterium bovis, the agents of tuberculosis in humans and bovines, respectively, did not allow identifying any large DNA fragment with aberrant GC content, a genetic signature of DNA acquired through HGT, including pathogenicity islands (Cole et al. 1998; Brosch et al. 2002; Garnier et al. 2003). This feature is consistent with the natural reluctance of mycobacteria to exchange genetic material, even between individuals, as demonstrated by recent studies showing that present-day populations of M. tuberculosis and M. bovis derive from a clonal expansion of a single successful ancestor (Smith et al. 2003; Supply et al. 2003; Hirsh et al. 2004). However, a recent genetic study of ancestral Mycobacterium prototuberculosis species concluded that many intraspecies HGT events must have occurred in the progenitor of M. tuberculosis before the evolutionary bottleneck leading to emergence of the M. tuberculosis complex (Gutierrez et al. 2005), possibly from the Indian subcontinent (Filliol et al. 2006).
We have recently identified M. tuberculosis virulence genes involved in macrophage parasitism (V. Rosas-Magallanes, unpublished data) by signature-tagged transposon mutagenesis (Camacho et al. 1999). These genes are involved in one or more steps of host cell infection, including attachment to the cell surface, cell entry, intracellular trafficking, and inhibition of phagosome-lysosome fusion, as well as intracellular bacterial metabolism. One of these genes, Rv0986, forms an operon together with Rv0987 and Rv0988 and encodes an ATP-binding cassette (ABC) transporter involved in early interactions between the bacillus and host cells. Mycobacterium tuberculosis mutants inactivated in Rv0986 and Rv0987 show reduced ability to bind to macrophages and to inhibit phagosome-lysosome fusion in vitro (Pethe et al. 2004; V. Rosas-Magallanes, unpublished data). Here, we show that the Rv0986-8 operon is specific to the M. tuberculosis complex and to ancestral M. prototuberculosis species among actinobacteria. In addition, phylogenetic reconstruction and analyses of GC content, codon usage, 3:1 dinucleotide, and four-letter genomic signature strongly suggest that this operon was acquired by the M. tuberculosis ancestor through HGT from a -proteobacterium donor. These results identify for the first time a M. tuberculosis-specific HGT that most likely contributed to the emergence of species of the tuberculous complex as major pathogens. This study illustrates the importance of evolutionary networks of HGT in M. tuberculosis in our understanding of mycobacterial virulence.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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Mycobacteria Culture and Genomic DNA Extraction
Mycobacteria were grown at 37°C in Middlebrook 7H9 broth (Difco, Detroit, Mich.) supplemented with 10% oleic acid, albumin, dextran, catalase (OADC) (0.05% oleic acid, 5% bovine serum albumin fraction V, 2% dextrose, 0.004% beef catalase, 0.85% NaCl) and 0.05% Tween80 (Sigma, St. Louis, Mo.) or on agar Middlebrook 7H11 medium (Difco) supplemented with OADC. Transposon-mediated mutants of M. tuberculosis were cultured in the presence of kanamycin (20 µg/ml). Genomic DNA was extracted as previously described (Pelicic et al. 1997
).
Polymerase Chain Reaction Amplification and Sequencing
Polymerase chain reactions (PCRs) contained per reaction 5 µl of 10 x PCR buffer (600 mM Tris HCl pH 8.8, 20 mM MgCl2, 170 mM (NH4)2SO4, 100 mM ß-mercaptoethanol), 5 µl of 20 mM nucleotide mix, 200 nM of each primer, 5–50 ng of template DNA, 10% dimethyl sulfoxide, 1 unit Taq polymerase (Invitrogen, Carlsbad, Calif.), and sterile distilled water to 50 µl. Thermal cycling was performed on a PTC-100 amplifier (MJ Inc., Watertown, Mass.) with an initial denaturation step of 90 s at 95°C, followed by 35 cycles of 30 s at 95°C, 1 min at 58°C, and 4 min at 72°C. For sequencing reactions, 35 cycles (96°C for 30 s, 56°C for 15 s, 60°C for 4 min) were performed in a thermocycler (MJ Inc.), using 5 µl of the column purified (Qiagen, Hilden, Germany) PCR product together with 1.5 µl of Big Dye sequencing mix 3.1 (Applied Biosystems, Foster City, Calif.), 1.5 µl (2 µM) of primer, and 2 µl of 5 x buffer (Applied Biosystems). DNA was precipitated using 80 µl of 80% ethanol, centrifuged, rinsed with 70% ethanol, and dried. Reactions were dissolved in 15 µl of formamide/ethylenediaminetetraacetic acid and subjected to automated sequencing on a 3100 DNA sequencer (Applied Biosystems). Primers used to amplify and sequence genes from M. tuberculosis and M. prototuberculosis strains were the following: Rv0986-fl-1101764F (5'-GGGCTAGACTACCGCCGAA-3'), Rv0986-1101803F (5'-ATGAACCGGCAACCTATCGTT-3'), Rv0986-1101838F (5'-GAGCTGGACATTCCGAGAAG-3'), Rv0986-1102272R (5'-ATAGCGACCCGTTGTTGTTC-3'), Rv0986-1102379F (5'-ACCCGCCAAGCAGGTAAAAC-3'), Rv0986-1102464F (5'-GCGGCAGGTTGATACCTGC-3'), Rv0987-1102971F (5'-CCCAACGGTGTCGTGTTAAGC-3'), Rv0987-1103154F (5'-CAAGAGTTGTTCCATATGCCC-3'), Rv0987-1103778F (5'-TTTGGTTTGGGTAGCTTTGGT-3'), Rv0987-1103972F (5'-TATTGTGCGCTCGTTGAGTC-3'), Rv0987-1103993R (5'-GCGACTCAACGAGCGCAC-3'), Rv0987-1104407R (5'-GTGTTGTCGCGATACCATTG-3'), Rv0987-1104621F (5'-CAAGCCGCGTTCGCGGGTCGG-3'), Rv0987-1104861F (5'-TTCATTGAGACCGGCCTAATG-3'), Rv0988-1105144F (5'-TACTGGTTCTGACGCTGACG-3'), Rv0988-1105488F (5'-GCGATAAGTGATATTTCG-3'), Rv0988-1105788F (5'-ACTGTCAGTGTTAATGGC-3'), Rv0988-1105602R (5'-ACCAATCGTCTAGCCACACC-3'), and Rv0988-fl-1106353R (5'-GGTTTGCAGCGATATCACAAC-3'). Long PCR amplifications (between mscL and Rv0990cI genes) were realized with TaKaRa LA Taq (Takara Bio Inc., Kyoto, Japan) according to manufacturer's instructions, with 300 nM of primer mscLfwd (5'-CGCGAGAAACTCCTTGAATC-3') and Rv0990crev (5'-CTGCACTGAACACGCCATAC-3') to amplify a 6-kb DNA fragment. Amplification was realized in a thermocycler (MyCycler, BioRad, BioRad Laboratories, Richmond, Calif.) with an initial step of 60 sat 94°C, followed by 30 cycles of 10 sdenaturation at 98°C and 15 min annealing and elongation at 68°C, and a final elongation step of 10 min at 72°C.
Southern Blotting Analysis
Genomic DNAs were digested with BamHI, run in an agarose gel, and transferred onto nitrocellulose. Rv0988 was PCR amplified from genomic M. tuberculosis MT103 DNA using Rv0988pVV16F (5'-TACATATGAGAAAAGCAGGATTGACC-3') and Rv0988pVV16R (5'-TAAAGCTTAGACAGCCGTTGTACATAG-3') as primers. Southern blotting analysis was performed as described (Pelicic et al. 1997) using the Rv0988 amplicon as a probe. Hybridization was realized overnight at 65°C. Membranes were washed twice in 2 x standard saline citrate (SSC)/0.1% sodium dodecyl sulfate (SDS) for 15 min, once in 1 x SSC/0.1% SDS for 10 min, and twice in 0.5 x SSC/0.1% SDS for 15 min. 1 x SSC buffer contains 150 mM NaCl and 15 mM C6H5Na3O7 (pH 7.0). Positive control consisted of hybridization using M. tuberculosis MT103 16S cDNA as a probe.
Bioinformatics
Complete and incomplete genome sequences were retrieved from The Institute for Genomic Research and the Sanger Institute Web sites. Incomplete sequences were annotated, using GeneMark. Phylogenetic trees were constructed by the neighbor-joining method (JTT distance calculation) from the amino acid sequences of Rv0988 and of its nearest neighbors after ClustalW alignment. GC content was calculated with GeneGC, using a window size of 900 nt and a step size of 51 nt. Genomic codon usage was retrieved from codon usage tabulated from GenBank. Frequencies in M. tuberculosis gene clusters were calculated with CodonW. Mean differences (%) from genomic codon usage were calculated with the Graphical Codon Usage Analyzer. We calculated 3:1 dinucleotide frequencies in the M. tuberculosis whole genome and individual genes with CodonW. Ka/Ks tests (Kimura 1968) were performed using the DnaSP package (Rozas et al. 2003). We also assessed the typicality of the operon by analyzing its four-letter word signature (Deschavanne et al. 1999; Dufraigne et al. 2005). The frequencies of the words found in a given sequence can be displayed in the form of a square image in which each pixel is associated with a specific oligonucleotide (word). The location of a given word is determined by means of an iterative procedure. The image is therefore divided into four quadrants (C, G, A, T), containing the appropriate nucleotides. This gives the base composition of the sequence. The quadrants were chosen such that the lower (A + T) and upper (G + C) halves indicate the base composition and the diagonals, the purine/pyrimidine composition. Each quadrant was subsequently divided into four subquadrants, each containing dinucleotides ending with the nucleotide of the main quadrant. Thus, dinucleotides differing only in their first letter were in adjacent subquadrants. This operation was performed on each subquadrant, to obtain trinucleotide frequencies, and the analysis was then extended to tetranucleotides. The color scale indicates the relative frequency per image of each word: the darker the color, the higher the frequency. The potential origin of the operon was determined by comparison of the operon signature (Dufraigne et al. 2005) with a bank of signatures from 22,655 species (including viruses and plasmids). A distance tree was inferred by the neighbor-joining method, from the signatures of M. tuberculosis, the Rv0986-8 operon, and their nearest neighbors.
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Results and Discussion |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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Mycobacterium tuberculosis Rv0986-8 is Orthologous to A. tumefaciens attE–H
Recent genetic screenings, including one by signature-tagged transposon mutagenesis, showed that Rv0986 plays a critical role in the ability of M. tuberculosis to infect host phagocytic cells (Pethe et al. 2004
; V. Rosas-Magallanes, unpublished data). Rv0986 encodes a putative adenosine triphosphate–binding protein sharing similarity with the Agrobacterium tumefaciens attE polypeptide (fig. 1A) and predicted to form an ABC transporter together with Rv0987 (Braibant, Gilot, and Content 2000). In A. tumefaciens, an 
-proteobacterium responsible for crown gall in plants, the plasmid-borne attE–H operon, is thought to encode an ABC transporter involved in the secretion of a host cell adhesion factor (Matthysse, Yarnall, and Young 1996; Matthysse et al. 2000). Interestingly, the Rv0987 N- and C-terminal sequences share 40% similarity with attF and attG, respectively, and the contiguous gene Rv0988 exhibits 50% similarity with attH (fig. 1A). Because Agrobacterium and Mycobacterium are two phylogenetically distant genera, we sought to investigate the evolutionary history of the Rv096-8 operon in more detail.
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Rv0986-8 is Specific to the M. tuberculosis Complex and Ancestral M. prototuberculosis Species Among Actinobacteria
We first determined whether this operon was present or absent in other mycobacterial species. PCR amplification using primers within the operon-flanking genes mscL and Rv0990c (fig. 1B) and Southern blot analysis using Rv0988 as a probe (fig. 1C) strongly suggested that this operon was specific to the M. tuberculosis complex, including M. tuberculosis, M. bovis, Mycobacterium africanum, and Mycobacterium microti (fig. 1D). In silico analysis of the available mycobacterial genomes further supported this hypothesis. Indeed, all the genes surrounding the operon, with the exception of grcC2, were detected in all mycobacteria examined. The Rv0986-8 operon, together with grcC2, which probably resulted from M. tuberculosis complex-specific duplication of the polyprenyl pyrophosphate synthase-encoding gene grcC1, were restricted to slow-growing species of the M. tuberculosis complex. These observations strongly suggest that the Rv0986-8 is indeed specific to the M. tuberculosis complex and that the operon was acquired through HGT. As Rv0986-8 was also detected in Mycobacterium canetti (fig. 1B and D), which has been recently proposed to be reclassified together with ancestral M. prototuberculosis species (Gutierrez et al. 2005
), we evaluated whether the operon was absent or present in M. prototuberculosis species. PCR amplification showed that all strains (A–I) of M. prototuberculosis possess the operon. Sequencing of the Rv0986-8 orthologues in these strains allowed us to quantify the number of synonymous and nonsynonymous mutations, as compared to the genes in M. tuberculosis H37Rv (tables 1 and 2). Ka/Ks analyses indicated a deficit in nonsynonymous mutations for the three genes (Ka/Ks values of 0.134 in average for Rv0986 and 0.264 in average for Rv0987 and Rv0988)—suggesting the presence of a selective constraint preserving the accumulation of amino acid changes over time. These observations point therefore to an important role of the operon in the evolutionary history of the tubercle bacillus.
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The Rv0986-8 Gene Cluster Has Been Acquired by HGT
In order to further investigate the HGT hypothesis and to eventually assign donor species to the operon, we next proceeded for additional in silico analyses. Blast analysis of Rv0988 identified orthologues of the protein exclusively in environmental and phylogenetically distant proteobacteria. Phylogenetic analyses were performed on the Rv0988 orthologues identified. In contrast with the 16S RNA-based phylogeny of Eubacteria, Rv0988 clustered with orthologues from proteobacteria (fig. 2). In proteobacteria, examination of the corresponding genomic regions showed that the Rv0986-8 orthologues were always physically linked, suggesting a unique event of HGT involving all these orthologues. Analysis of the mprA-Rv0992c region revealed that the GC content of the Rv0986-8 operon was only about 53%, whereas that observed in the flanking regions was about 66%, which is in the range observed for the global M. tuberculosis genome (fig. 3A). GC content at the first and third positions in the codons showed the greatest deviation from that in flanking genes and, generally, in the genome as a whole (Table S1, Supplementary Material online). Consequently, codon usage in Rv0986-8 differed by a mean of 18.7% from that of M. tuberculosis, whereas a difference of
5% was observed for the flanking genes (fig. 3B). Furthermore, analysis of the bias in 3:1 (third and successive first bases) dinucleotides, which are subject to the weakest selective constraints and in which mutational events are therefore more tolerated, showed that the bias in Rv0986-8 with respect to the entire coding genome was much greater than that in the flanking genes (fig. 3C and Table S2, Supplementary Material online). These results strongly suggest that the Rv0986-8 operon was acquired horizontally by the ancestor of M. tuberculosis.
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Genomic Signature Analysis Identifies
-Proteobacteria as Possible Rv0986-8 DonorsBased on the analysis of four-letter genomic signatures (words), a powerful method has been recently developed for the identification of possible donors of genes acquired through HGT (Dufraigne et al. 2005
). We applied this method to compare the genomic signature of the Rv0986-8 operon with those of DNAs from over 22,000 species, including bacteria, phages, viruses, and plasmids. Consistent with the results presented above, the signature within the operon was highly incongruent with that of the M. tuberculosis genome (fig. 4A) and clustered primarily with sequences from proteobacteria (>76% of the closest species, fig. 4B) and more particularly from -proteobacteria (
62%, fig. 4A and B). Interestingly, 30% of the most closely related sequences are plasmid borne, suggesting a possible plasmid-mediated transfer. The species at closest genomic distances from Rv0986-8 are listed in table 3. Again, the majority of the most closely related sequences were from -proteobacteria.
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A previous microarray-based screening study of M. tuberculosis genes induced in vivo has identified a 34-kb DNA fragment encompassing several operons, including Rv0986-8 (Talaat et al. 2004
). Based on its GC content (<55%), it has been suggested that the whole 34-kb gene cluster may have arisen through transposition. Our data clearly show that the transferred segment contains only the Rv0986-8 operon and was probably generated by plasmid-mediated HGT from a -proteobacterium to the M. tuberculosis/M. prototuberculosis common ancestor. In this view, our results provide a mechanism and temporal scenario for this genetic event and show for the first time that HGT has likely contributed to the emergence of M. tuberculosis and related strains of the M. tuberculosis complex. |
Conclusion |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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Our results strongly support the hypothesis that the ancestor of the M. tuberculosis complex may have been, like Mycobacterium marinum and most mycobacteria, an early environmental species that subsequently colonized eukaryotes. The acquisition of Rv0986-8 and of other genes presumably conferred a selective advantage to this ancestor, making it possible to colonize plants or lower animals, such as prototype M
s (amoebae). These genes may have been subsequently used by species of the complex to facilitate the colonization of other cells (mammalian cells). In this view, it is tempting to hypothesize that the acquisition of the Rv0986-8 operon may have increased the fitness of the M. tuberculosis population, being therefore subject to positive selection. Global in silico studies have recently suggested that HGT may not be as rare as previously thought in M. tuberculosis. For example, a total of 176 and 442 M. tuberculosis open reading frames, including Rv0986 and Rv0988, are thought to be "alien" genes, based on an analysis of GC content (Garcia-Vallve et al. 2003) and Bayesian inferences in training models for nucleotide composition (Nakamura et al. 2004), respectively. The future comparison of the genomes of M. tuberculosis and closely related species, such as M. prototuberculosis and M. marinum, may make it possible to identify other cases of horizontal transfer of genes involved in M. tuberculosis virulence and interactions with host cells. In this search, genomic signature analysis (Dufraigne et al. 2005) may prove useful, particularly for the identification of possible donors and for improving our understanding of the microbial environment in which the M. tuberculosis complex emerged. |
Supplementary Material |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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Supplementary Tables S1 and S2 are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionSupplementary MaterialAcknowledgementsReferences |
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This work was supported by Institut Pasteur and the European Community (contract numbers QLK2-CT-2001-02018 and QLK2-CT-2000-01761). V.R.M. is a fellow of Conacyt and Fondation pour la Recherche Médicale. We thank D. G. Russell (Ithaca, United States), G. R. Stewart (London, United Kingdom), E. Rocha (Paris, France) for helpful discussions and critical reading of the manuscript and V. Vincent (Paris, France) for providing mycobacterial strains. M. marinum sequence data were produced by the M. marinum Sequencing Group at the Sanger Institute and can be obtained from ftp://ftp.sanger.ac.uk/pub/M_marinum. Preliminary M. smegmatis and M. avium sequence data was obtained from The Institute for Genomic Research website at http://www.tigr.org. Sequencing of M. smegmatis and M. avium was accomplished with support from the National Institute of Allergy and Infectious Diseases.
Funding to pay the Open Access publication charges for this article was provided by Institut Pasteur.
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Footnotes |
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William Martin, Associate Editor
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References |
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Blanc-Potard, A. B., and B. Lafay. 2003. MgtC as a horizontally-acquired virulence factor of intracellular bacterial pathogens: evidence from molecular phylogeny and comparative genomics. J. Mol. Evol. 57:479–486.[CrossRef][Medline]
Boucher, Y., C. J. Douady, R. T. Papke, D. A. Walsh, M. E. Boudreau, C. L. Nesbo, R. J. Case, and W. F. Doolittle. 2003. Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37:283–328.[CrossRef][ISI][Medline]
Braibant, M., P. Gilot, and J. Content. 2000. The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol. Rev. 24:449–467.[CrossRef][ISI][Medline]
Brosch, R., S. V. Gordon, M. Marmiesse et al. (15 co-authors). 2002. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl. Acad. Sci. USA 99:3684–3689.
Camacho, L. R., D. Ensergueix, E. Perez, B. Gicquel, and C. Guilhot. 1999. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 34:257–267.[CrossRef][ISI][Medline]
Cole, S. T., R. Brosch, J. Parkhill et al. (42 co-authors). 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544.[CrossRef][Medline]
Deschavanne, P. J., A. Giron, J. Vilain, G. Fagot, and B. Fertil. 1999. Genomic signature: characterization and classification of species assessed by chaos game representation of sequences. Mol. Biol. Evol. 16:1391–1399.[Abstract]
Dufraigne, C., B. Fertil, S. Lespinats, A. Giron, and P. Deschavanne. 2005. Detection and characterization of horizontal transfers in prokaryotes using genomic signature. Nucleic Acids Res. 33:e6.
Filliol, I., A. S. Motiwala, M. Cavatore et al. (25 co-authors). 2006. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J. Bacteriol. 188:759–772.
Garcia-Vallve, S., E. Guzman, M. A. Montero, and A. Romeu. 2003. HGT-DB: a database of putative horizontally transferred genes in prokaryotic complete genomes. Nucleic Acids Res. 31:187–189.
Garnier, T., K. Eiglmeier, J. C. Camus et al. (22 co-authors). 2003. The complete genome sequence of Mycobacterium bovis. Proc. Natl. Acad. Sci. USA 100:7877–7882.
Gutierrez, M. C., S. Brisse, R. Brosch, M. Fabre, B. Omais, M. Marmiesse, P. Supply, and V. Vincent. 2005. Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog. 1:e5.[Medline]
Hirsh, A. E., A. G. Tsolaki, K. DeRiemer, M. W. Feldman, and P. M. Small. 2004. Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc. Natl. Acad. Sci. USA 101:4871–4876.
Jain, R., M. C. Rivera, J. E. Moore, and J. A. Lake. 2003. Horizontal gene transfer accelerates genome innovation and evolution. Mol. Biol. Evol. 20:1598–1602.
Kimura, M. 1968. Evolutionary rate at the molecular level. Nature 217:624–626.[CrossRef][Medline]
Kinsella, R. J., D. A. Fitzpatrick, C. J. Creevey, and J. O. McInerney. 2003. Fatty acid biosynthesis in Mycobacterium tuberculosis: lateral gene transfer, adaptive evolution, and gene duplication. Proc. Natl. Acad. Sci. USA 100:10320–10325.
Martin, C., J. Timm, J. Rauzier, R. Gomez-Lus, J. Davies, and B. Gicquel. 1990. Transposition of an antibiotic resistance element in mycobacteria. Nature 345:739–743.[CrossRef][Medline]
Matthysse, A. G., H. Yarnall, S. B. Boles, and S. McMahan. 2000. A region of the Agrobacterium tumefaciens chromosome containing genes required for virulence and attachment to host cells. Biochim. Biophys. Acta 1490:208–212.[Medline]
Matthysse, A. G., H. A. Yarnall, and N. Young. 1996. Requirement for genes with homology to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J. Bacteriol. 178:5302–5308.
Nakamura, Y., T. Itoh, H. Matsuda, and T. Gojobori. 2004. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat. Genet. 36:760–766.[CrossRef][ISI][Medline]
Ochman, H., J. G. Lawrence, and E. A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304.[CrossRef][Medline]
Pelicic, V., M. Jackson, J. M. Reyrat, W. R. Jacobs, Jr., B. Gicquel, and C. Guilhot. 1997. Efficient allelic exchange and transposon mutagenesis in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 94:10955–10960.
Pethe, K., D. L. Swenson, S. Alonso, J. Anderson, C. Wang, and D. G. Russell. 2004. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc. Natl. Acad. Sci. USA 101:13642–13647.
Philippe, H., and C. J. Douady. 2003. Horizontal gene transfer and phylogenetics. Curr. Opin. Microbiol. 6:498–505.[CrossRef][ISI][Medline]
Rozas, J., J. C. Sanchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497.
Smith, N. H., J. Dale, J. Inwald, S. Palmer, S. V. Gordon, R. G. Hewinson, and J. M. Smith. 2003. The population structure of Mycobacterium bovis in Great Britain: clonal expansion. Proc. Natl. Acad. Sci. USA 100:15271–15275.
Supply, P., R. M. Warren, A. L. Banuls, S. Lesjean, G. D. Van Der Spuy, L. A. Lewis, M. Tibayrenc, P. D. Van Helden, and C. Locht. 2003. Linkage disequilibrium between minisatellite loci supports clonal evolution of Mycobacterium tuberculosis in a high tuberculosis incidence area. Mol. Microbiol. 47:529–538.[CrossRef][Medline]
Talaat, A. M., R. Lyons, S. T. Howard, and S. A. Johnston. 2004. The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc. Natl. Acad. Sci. USA 101:4602–4607.
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 J. Becq, M. C. Gutierrez, V. Rosas-Magallanes, J. Rauzier, B. Gicquel, O. Neyrolles, and P. Deschavanne Contribution of Horizontally Acquired Genomic Islands to the Evolution of the Tubercle Bacilli Mol. Biol. Evol., August 1, 2007; 24(8): 1861 - 1871. [Abstract] [Full Text] [PDF]
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|
|
|
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 T. Dagan and W. Martin Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution PNAS, January 16, 2007; 104(3): 870 - 875. [Abstract] [Full Text] [PDF]
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|
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 V. Rosas-Magallanes, G. Stadthagen-Gomez, J. Rauzier, L. B. Barreiro, L. Tailleux, F. Boudou, R. Griffin, J. Nigou, M. Jackson, B. Gicquel, et al. Signature-Tagged Transposon Mutagenesis Identifies Novel Mycobacterium tuberculosis Genes Involved in the Parasitism of Human Macrophages Infect. Immun., January 1, 2007; 75(1): 504 - 507. [Abstract] [Full Text] [PDF]
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