Abstract
The genome of about 10% of bacterial species is divided among two or more large chromosome-sized replicons. The contribution of each replicon to the microbial life cycle (for example, environmental adaptations and/or niche switching) remains unclear. Here we report a genome-scale metabolic model of the legume symbiont Sinorhizobium meliloti that is integrated with carbon utilization data for 1,500 genes with 192 carbon substrates. Growth of S. meliloti is modelled in three ecological niches (bulk soil, rhizosphere and nodule) with a focus on the role of each of its three replicons. We observe clear metabolic differences during growth in the tested ecological niches and an overall reprogramming following niche switching. In silico examination of the inferred fitness of gene deletion mutants suggests that secondary replicons evolved to fulfil a specialized function, particularly host-associated niche adaptation. Thus, genes on secondary replicons might potentially be manipulated to promote or suppress host interactions for biotechnological purposes.
Highlights
The genome of about 10% of bacterial species is divided among two or more large chromosome-sized replicons
The last years have witnessed a growing attention towards the ecological and evolutionary implication of the multiple replicon bacterial genome[1,2,3,4] that is present in about 10% of sequenced bacterial genomes[1]. This genome architecture is common in the proteobacterial species that interact with a host and are of importance to the human population[1,2], including crop plant symbionts, plant pathogens, and animal and human pathogens
We combine a genome-scale metabolic network reconstruction of the S. meliloti genome, flux balance analysis (FBA), and growth phenotype data for 11 large-scale S. meliloti deletion mutants to examine the metabolic changes accompanying the shifts between bulk soil, rhizosphere and nodule environments
Summary
The genome of about 10% of bacterial species is divided among two or more large chromosome-sized replicons. Several recent studies have provided evidence consistent with the secondary replicons in a multipartite genome encoding environment-specific fitness promoting but non-essential functions[3,4,8,9,10,11,12]. Sinorhizobium meliloti is a N2-fixing endosymbiont of legume species that has recently become a model organism for the study of bacterial multipartite genome function and evolution. We combine a genome-scale metabolic network reconstruction of the S. meliloti genome, flux balance analysis (FBA), and growth phenotype data for 11 large-scale S. meliloti deletion mutants to examine the metabolic changes accompanying the shifts between bulk soil, rhizosphere and nodule environments. We use an in silico approach to predict the phenotypes resulting from the deletion of 1,575 S. meliloti metabolic genes, estimate the fitness contribution of each replicon within each environment, and provide insight into the evolution of multipartite genomes. IGD1575 is the first metabolic model capable of representing the metabolism of both a symbiotic and free-living rhizobial cell
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