Mycobacterial phylogenomics: an enhanced method for gene turnover analysis reveals uneven levels of gene gain and loss among species and gene families

TY - JOUR

T1 - Mycobacterial phylogenomics

T2 - an enhanced method for gene turnover analysis reveals uneven levels of gene gain and loss among species and gene families

AU - Librado, Pablo

AU - Garrett Vieira, Filipe Jorge

AU - Sánchez-Gracia, Alejandro

AU - Kolokotronis, Sergios Orestis

AU - Rozas, Julio

PY - 2014/6

Y1 - 2014/6

N2 - 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.

AB - 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.

KW - gene families

KW - gene gain and loss

KW - gene turnover rates

KW - M. tuberculosis

KW - maximum likelihood

KW - rate heterogeneity

UR - http://www.scopus.com/inward/record.url?scp=84925884132&partnerID=8YFLogxK

U2 - 10.1093/gbe/evu117

DO - 10.1093/gbe/evu117

M3 - Journal article

C2 - 24904011

AN - SCOPUS:84925884132

SN - 1759-6653

VL - 6

SP - 1454

EP - 1465

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

IS - 6

ER -