Comparative functional pan-genome analyses to build connections between genomic dynamics and phenotypic evolution in polycyclic aromatic hydrocarbon metabolism in the genus Mycobacterium

Abstract

BackgroundThe bacterial genus Mycobacterium is of great interest in the medical and biotechnological fields. Despite a flood of genome sequencing and functional genomics data, significant gaps in knowledge between genome and phenome seriously hinder efforts toward the treatment of mycobacterial diseases and practical biotechnological applications. In this study, we propose the use of systematic, comparative functional pan-genomic analysis to build connections between genomic dynamics and phenotypic evolution in polycyclic aromatic hydrocarbon (PAH) metabolism in the genus Mycobacterium.ResultsPhylogenetic, phenotypic, and genomic information for 27 completely genome-sequenced mycobacteria was systematically integrated to reconstruct a mycobacterial phenotype network (MPN) with a pan-genomic concept at a network level. In the MPN, mycobacterial phenotypes show typical scale-free relationships. PAH degradation is an isolated phenotype with the lowest connection degree, consistent with phylogenetic and environmental isolation of PAH degraders. A series of functional pan-genomic analyses provide conserved and unique types of genomic evidence for strong epistatic and pleiotropic impacts on evolutionary trajectories of the PAH-degrading phenotype. Under strong natural selection, the detailed gene gain/loss patterns from horizontal gene transfer (HGT)/deletion events hypothesize a plausible evolutionary path, an epistasis-based birth and pleiotropy-dependent death, for PAH metabolism in the genus Mycobacterium. This study generated a practical mycobacterial compendium of phenotypic and genomic changes, focusing on the PAH-degrading phenotype, with a pan-genomic perspective of the evolutionary events and the environmental challenges.ConclusionsOur findings suggest that when selection acts on PAH metabolism, only a small fraction of possible trajectories is likely to be observed, owing mainly to a combination of the ambiguous phenotypic effects of PAHs and the corresponding pleiotropy- and epistasis-dependent evolutionary adaptation. Evolutionary constraints on the selection of trajectories, like those seen in PAH-degrading phenotypes, are likely to apply to the evolution of other phenotypes in the genus Mycobacterium.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0302-8) contains supplementary material, which is available to authorized users.

Tracking the Taxonomy of the Genus Bifidobacterium Based on a Phylogenomic Approach

“…Pangenome reconstruction among members of the genus Bifidobacterium. Recently, species-and genus-level comparative genomic analyses based on pangenome reconstruction have been shown to be crucial in providing information regarding the overall gene content, while also generating information on the resistome, metabolic capabilities, and mobilome of such taxonomic ranks (9,(24)(25)(26)(27)(28). In recent years, the number of sequenced bifidobacterial strains has increased from a few dozen to several hundred, and thus we felt it was opportune to explore the genomic biodiversity within different species of the genus Bifidobacterium (12,15,16,29).…”

Implications of microbial adaptation for the assessment of environmental persistence of chemicals

“…These genes are widespread and can be easily transferred across the whole community by HGT (also referred to as lateral gene transfer). HGT plays an important role in fitness and adaptation of bacterial communities in contaminated environments (Kweon et al, 2015;Top & Springael, 2003). Under particular conditions, individual cells that were involved in HGT events may be positively selected and expand the basis of bacterial adaptation (Nielsen, Bøhn, & Townsend, 2014).…”

“…However, a vast majority of HGT events in communities will be lost due to lack of replication success of the transferred material (Nielsen et al, 2014). The importance of gene transfer for adaptation to new compounds has been investigated in many studies (Janssen, Dinkla, Poelarends, & Terpstra, 2005;van der Meer et al, 1992) and these events have been observed for the breakdown of many compounds, such as chlorobenzene (van der Meer, 2006), atrazine (Aislabie, Bej, Ryburn, Lloyd, & Wilkins, 2005;de Souza et al, 1998;Janssen et al, 2005;Rousseaux, Soulas, & Hartmann, 2002), hexachlorocyclohexanes (van der Meer, 2006), other halogenated molecules (Janssen et al, 2005) and polycyclic aromatic hydrocarbons (PAHs) (Kweon et al, 2015).…”

Aerobic bacteria degrading both n-alkanes and aromatic hydrocarbons: an undervalued strategy for metabolic diversity and flexibility

“…The names of strains mentioned in the text were marked in bold Table 1). The broadly distributed PAH-degrading capacities among mycobacteria have probably resulted from extensive HGT (horizontal gene transfer) events in genomic regions that contain genes for HMW PAHs (high molecular weight PAHs) metabolism (Kweon et al 2015). Principally, the utilization of aromatic compounds was demonstrated, while the capabilities of n-alkane degradation were not reported in many cases.…”