Mycobacterial Phylogenomics: An Enhanced Method for Gene Turnover Analysis Reveals Uneven Levels of Gene Gain and Loss among Species and Gene Families

Abstract

Species of the genus Mycobacterium differ in several features, from geographic ranges, and degree of pathogenicity, to ecological and host preferences. The recent availability of several fully sequenced genomes for a number of these species enabled the comparative study of the genetic determinants of this wide lifestyle diversity. Here, we applied two complementary phylogenetic-based approaches using information from 19 Mycobacterium genomes to obtain a more comprehensive view of the evolution of this genus. First, we inferred the phylogenetic relationships using two new approaches, one based on a Mycobacterium-specific amino acid substitution matrix and the other on a gene content dissimilarity matrix. Then, we utilized our recently developed gain-and-death stochastic models to study gene turnover dynamics in this genus in a maximum-likelihood framework. We uncovered a scenario that differs markedly from traditional 16S rRNA data and improves upon recent phylogenomic approaches. We also found that the rates of gene gain and death are high and unevenly distributed both across species and across gene families, further supporting the utility of the new models of rate heterogeneity applied in a phylogenetic context. Finally, the functional annotation of the most expanded or contracted gene families revealed that the transposable elements and the fatty acid metabolism-related gene families are the most important drivers of gene content evolution in Mycobacterium.

Gene Turnover Contributes to the Evolutionary Adaptation of Acidithiobacillus caldus: Insights from Comparative Genomics

“…As stated by Carretero-Paulet et al (2015), homologous genes derived from newly formed subgenomes might undergo asymmetric fractionation via mutational events, which include nucleotide substitutions, gene gains and losses, and changes in genomic structure and organization (Librado et al, 2014). In terms of neutral mutation theory, mutations underlying gene and genome evolution, though not necessarily beneficial, should accumulate at a constant rate by drift (Kimura, 1984).…”

“…Only in recent decades has great attention been paid to the molecular mechanisms of gene loss (deletion or pseudogenization) as a pervasive source of genetic change, which is believed to be another key evolutionary event that causes adaptive phenotypic diversity (Albalat and Cañestro, 2016). In recent years, a number of analytical methods for population genomics and molecular evolution have provided substantial evidence to determine the relative contribution of diverse evolutionary forces, which shape genome organization, architecture, and diversity in response to environmental perturbations (Librado et al, 2014). In eukaryotes, gene family evolution has often been modeled after a phylogenetic birth-and-death (BD) process (Nei and Rooney, 2005).…”

“…In eukaryotes, gene family evolution has often been modeled after a phylogenetic birth-and-death (BD) process (Nei and Rooney, 2005). This BD model, though suitable to account for single-gene duplications, might not be appropriate for calculating gene turnover rates given that horizontal gene transfer (HGT) events occur in certain organisms (Librado et al, 2014). However, an alternative gain-and-death (GD) stochastic model in a maximum-likelihood statistical framework was applied to circumvent this limitation (Librado et al, 2012).…”

“…However, an alternative gain-and-death (GD) stochastic model in a maximum-likelihood statistical framework was applied to circumvent this limitation (Librado et al, 2012). Unlike the birth process, gains in the developed GD model can accommodate all kinds of gene acquisitions, irrespective of their original source, even including HGT (Librado et al, 2014). In this study, we are interested in whether the aforementioned theoretical and analytical approaches can be applied to explain the relationship between genetic change and adaptive evolution of A. caldus inhabiting extraordinarily extreme environments.…”

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

“…Recently, large-scale studies based on increasing genomic data have significantly expanded the spectrum of genome reduction into a pervasive source of genetic modifications that potentially cause adaptive phenotypic diversity (10). Extensive gene loss events were observed across a wide range of organisms, including prokaryotes (11)(12)(13)(14)(15), protists (16), fungi (17,18), plants (19), and even animals (20)(21)(22)(23), thereby serving as robust evidence to support the pervasiveness of gene loss in all life kingdoms (10). However, the relative contributions of different evolutionary forces that shape the organization, structure, and diversification of microbial genomes remain elusive.…”