Abstract
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.
Highlights
Assessing how mycobacteria acquire and maintain the genetic variation needed to both adapt to host immunity and to evolve drug resistance is of paramount importance in efforts to eradicate diseases such as tuberculosis and leprosy
For the three mycobacterial species above that showed affinities to other lineages (M. abscessus to Segniliparus, and M. smegmatis and M. vanbaalenii to Streptomyces), we examined the distribution of patristic distances for three sets of genes: (i) genes found only in a single mycobacterial species, with the other lineage as closest partner; (ii) genes found in more than one mycobacterial species and the other lineage, with no requirement that the other lineage be the closest partner; and (iii) genes found in the mycobacterial species and a close comparator species from the same genus
One of the most problematic aspects of reconstructing bacterial evolutionary histories using phylogenetic and comparative genomic analyses is the chance that horizontal gene transfer (HGT) renders two sequences similar not because the organisms share a recent common ancestor, but because one or both taxa have horizontally acquired a genomic segment from another distantly related species
Summary
Assessing how mycobacteria acquire and maintain the genetic variation needed to both adapt to host immunity and to evolve drug resistance is of paramount importance in efforts to eradicate diseases such as tuberculosis and leprosy. The raw material upon which natural selection operates, is especially important in species inhabiting rapidly changing environments as it ensures the existence of genetic variants with potential adaptations to a wide range of possible growth conditions. It is very important, that following an environmental change and the subsequent outgrowth of individuals carrying the appropriate adaptive mutations, mechanisms exist whereby population-wide genetic diversity is either preserved or is rapidly reestablished before the environmental shift occurs. For example, high mutation rates can ensure the reestablishment of novel genetic variation, high rates of genetic recombination coupled with selection can permit the spread of adaptive mutations throughout a population and, in so doing, preserve populationwide genetic diversity following environmental changes [4,5,6,7]
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