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

Ohgew Kweon,Jochen Blom,Carl E Cerniglia,John B Sutherland,Sung-Kwan Kim,Dong-Heon Baek,Su Inn Park,Seong-Jae Kim,Bong-Soo Kim

doi:10.1186/s12862-015-0302-8

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.

Highlights

The bacterial genus Mycobacterium is of great interest in the medical and biotechnological fields
Functional pan-genomic view of the six Polycyclic aromatic hydrocarbons (PAHs)-degraders with PAH-degrading phenotype in the mycobacterial phenotype network (MPN) For functional pan-genomic understanding of the PAHdegrading phenotype, we investigated the pan-genome of the six PAH-degrading mycobacteria in the ‘PAH-degrading’ node based on the previous proteomic data from M. vanbaalenii PYR-1 [9]
Taking the whole picture into account, mycobacterial PAH metabolism at the genus level might be an excellent phenotypic model to bridge genomic dynamics and phenotypic evolution, which could address a series of questions for a predictable direction and plausible trajectories for mycobacterial evolution

Summary

Introduction

The bacterial genus Mycobacterium is of great interest in the medical and biotechnological fields. There has been great interest in mycobacteria due to their abilities both to cause devastating diseases in humans and animals and to degrade toxic compounds in the environment [4,5] For these reasons, the number of available genome sequences has been growing fast and genome-scale omics data have been generated, allowing deeper functional genomics insights into their phenotypic features [6,7,8,9,10,11,12,13]. Despite the exciting discoveries continually adding to the broader and deeper knowledge of mycobacteria, there is a significant knowledge gap between genome and phenome in the genus Mycobacterium, due mainly to the epistatic and pleiotropic complexity of the genomic and phenotypic traits. The epistatic interaction—functional combination of two or more genes (or enzymes) for a single trait (or phenotype)—and pleiotropic activity—functional contribution of a gene (or enzyme) for multiple traits (or phenotypes)—are still poorly understood at the genome level [16] but are essential for a deeper understanding of mycobacterial systems

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