Insights into the evolutionary history of tubercle bacilli as disclosed by genetic rearrangements within a PE_PGRS duplicated gene pair

Karboul, Anis; Pittius, Nicolaas C. Gey van; Namouchi, Amine; Vincent, Véronique; Sola, Christophe; Rastogi, Nalin; Suffys, Philip Noël; Fabre, M.; Cataldi, Angel; Huard, Richard C.; Kurepina, Natalia; Kreiswirth, Barry N.; Ho, John L.; Gutiérrez, M. Cristina; Mardassi, Helmi

doi:10.1186/1471-2148-6-107

Cited by 41 publications

(23 citation statements)

References 58 publications

(65 reference statements)

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“…Of particular interest, the highly repetitive subfamilies PE_PGRS and PPE_MPTR expanded only in the genome of the MTBC members and close relatives. Consistently, we have also identified a polymorphism in a duplicated PE_PGRS gene pair, whose distribution through members of the MTBC, and several other mycobacterial species, provided an evolutionary history that conforms to the established scenario and confirmed the ancient origin of the smooth tubercle bacillus, M. canettii [22].…”

Section: Introductionsupporting

confidence: 80%

“…Indeed, PE/PE_PGRS genes share extensive homologous regions which make them more prone to recombination than any other sequences [7]. We have previously reported on the occurrence of such rearrangements in MTBC strains either via gene conversion [22], involving neighboring PE_PGRS genes, or through intragenic and/or intergenic homologous recombination events [28]. In the present study we provide evidence for the occurrence of both types of recombination in STB.…”

Section: Discussionsupporting

confidence: 59%

“…Such a mechanism may be of importance for PE/PE_PGRS duplicates in particular. In a previous study we showed that PE_PGRS17 has acquired, most likely through horizontal gene transfer in the ancestor clone, a new DNA stretch which is then transferred to its neighboring paralogue, PE_PGRS18, through gene conversion [22]. We demonstrated that the reverse mechanism could take place naturally resulting in the elimination of the acquired DNA stretch from the PE_PGRS17 copy, thus restoring its original sequence.…”

Section: Discussionmentioning

confidence: 73%

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Evolution of Smooth Tubercle Bacilli PE and PE_PGRS Genes: Evidence for a Prominent Role of Recombination and Imprint of Positive Selection

et al. 2013

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BackgroundPE and PE_PGRS are two mycobateria-restricted multigene families encoding membrane associated and secreted proteins that have expanded mainly in the pathogenic species, notably the Mycobacterium tuberculosis complex (MTBC). Several lines of evidence attribute to PE and PE_PGRS genes critical roles in mycobacterial pathogenicity. To get more insight into the nature of these genes, we sought to address their evolutionary trajectories in the group of smooth tubercle bacilli (STB), the putative ancestor of the clonal MTBC.Methodology/Principal FindingsBy focussing on six polymorphic STB PE/PE_PGRS genes, we demonstrate significant incongruence among single gene genealogies and detect strong signals of recombination using various approaches. Coalescent-based estimation of population recombination and mutation rates (ρ and θ, respectively) indicates that the two mechanisms are of roughly equal importance in generating diversity (ρ/θ = 1.457), a finding in a marked contrast to house keeping genes (HKG) whose evolution is chiefly brought about by mutation (ρ/θ = 0.012). In comparison to HKG, we found 15 times higher mean rate of nonsynonymous substitutions, with strong evidence of positive selection acting on PE_PGRS62 (dN/dS = 1.42), a gene that has previously been shown to be essential for mycobacterial survival in macrophages and granulomas. Imprint of positive selection operating on specific amino acid residues or along branches of PE_PGRS62 phylogenetic tree was further demonstrated using maximum likelihood- and covarion-based approaches, respectively. Strikingly, PE_PGR62 proved highly conserved in present-day MTBC strains.Conclusions/SignificanceOverall the data indicate that, in STB, PE/PE_PGRS genes have undergone a strong diversification process that is speeded up by recombination, with evidence of positive selection. The finding that positive selection involved an essential PE_PGRS gene whose sequence appears to be driven to fixation in present-day MTBC strains lends further support to the critical role of PE/PE_PGRS genes in the evolution of mycobacterial pathogenicity.

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Section: Introductionsupporting

confidence: 80%

Section: Discussionsupporting

confidence: 59%

Section: Discussionmentioning

confidence: 73%

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Evolution of Smooth Tubercle Bacilli PE and PE_PGRS Genes: Evidence for a Prominent Role of Recombination and Imprint of Positive Selection

et al. 2013

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“…PGRS is a highly polymorphic GC-rich sequence present in multiple sets of copies on the M. tuberculosis chromosome. The evolution of PGRS containing regions is due to duplication, recombination and strand slippage [29], however, these mutations rarely induce changes that can be observed in the PGRS-RFLP image [30]. It has been estimated that the rate of change of PGRS is slower than that of IS 6110 , however, exact estimates are not available [31].…”

Section: Genetic Markers In M Tuberculosismentioning

confidence: 99%

Genotyping of Mycobacterium Tuberculosis : Application in Epidemiologic Studies

Kato‐Maeda¹,

2011

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Genotyping is used to track specific isolates of Mycobacterium tuberculosis in a community. It has been successfully used in epidemiologic research (termed ‘molecular epidemiology’) to study the transmission dynamics of TB. In this article, we review the genetic markers used in molecular epidemiologic studies including the use of whole-genome sequencing technology. We also review the public health application of molecular epidemiologic tools.

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“…In some cases, the unique presence of a group of genes in one mycobacterial species is used as the starting point for further analyses, which in turn can include G+C content comparison of the unique genes with their flanking regions [18], and/or the characterization of a different class of enzymes [19] or protein subfamily [20] being encoded by the novel genes. Others have proposed the occurrence of HGT upon finding mobile and insertion elements, and/or genomic islands [21].…”

Section: Introductionmentioning

confidence: 99%

Comparative Genomic and Phylogenetic Approaches to Characterize the Role of Genetic Recombination in Mycobacterial Evolution

et al. 2012

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The genus Mycobacterium encompasses over one hundred named species of environmental and pathogenic organisms, including the causative agents of devastating human diseases such as tuberculosis and leprosy. The success of these human pathogens is due in part to their ability to rapidly adapt to their changing environment and host. Recombination is the fastest way for bacterial genomes to acquire genetic material, but conflicting results about the extent of recombination in the genus Mycobacterium have been reported. We examined a data set comprising 18 distinct strains from 13 named species for evidence of recombination. Genomic regions common to all strains (accounting for 10% to 22% of the full genomes of all examined species) were aligned and concatenated in the chromosomal order of one mycobacterial reference species. The concatenated sequence was screened for evidence of recombination using a variety of statistical methods, with each proposed event evaluated by comparing maximum-likelihood phylogenies of the recombinant section with the non-recombinant portion of the dataset. Incongruent phylogenies were identified by comparing the site-wise log-likelihoods of each tree using multiple tests. We also used a phylogenomic approach to identify genes that may have been acquired through horizontal transfer from non-mycobacterial sources. The most frequent associated lineages (and potential gene transfer partners) in the Mycobacterium lineage-restricted gene trees are other members of suborder Corynebacterinae, but more-distant partners were identified as well. In two examined cases of potentially frequent and habitat-directed transfer (M. abscessus to Segniliparus and M. smegmatis to Streptomyces), observed sequence distances were small and consistent with a hypothesis of transfer, while in a third case (M. vanbaalenii to Streptomyces) distances were larger. The analyses described here indicate that whereas evidence of recombination in core regions within the genus is relatively sparse, the acquisition of genes from non-mycobacterial lineages is a significant feature of mycobacterial evolution.

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Insights into the evolutionary history of tubercle bacilli as disclosed by genetic rearrangements within a PE_PGRS duplicated gene pair

Cited by 41 publications

References 58 publications

Evolution of Smooth Tubercle Bacilli PE and PE_PGRS Genes: Evidence for a Prominent Role of Recombination and Imprint of Positive Selection

Evolution of Smooth Tubercle Bacilli PE and PE_PGRS Genes: Evidence for a Prominent Role of Recombination and Imprint of Positive Selection

Genotyping of Mycobacterium Tuberculosis : Application in Epidemiologic Studies

Comparative Genomic and Phylogenetic Approaches to Characterize the Role of Genetic Recombination in Mycobacterial Evolution

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