Abstract
BackgroundGenome reduction is a common evolutionary process affecting bacterial lineages that establish symbiotic or pathogenic associations with eukaryotic hosts. Such associations yield highly reduced genomes with greatly streamlined metabolic abilities shaped by the type of ecological association with the host. Sodalis glossinidius, the secondary endosymbiont of tsetse flies, represents one of the few complete genomes available of a bacterium at the initial stages of this process. In the present study, genome reduction is studied from a systems biology perspective through the reconstruction and functional analysis of genome-scale metabolic networks of S. glossinidius.ResultsThe functional profile of ancestral and extant metabolic networks sheds light on the evolutionary events underlying transition to a host-dependent lifestyle. Meanwhile, reductive evolution simulations on the extant metabolic network can predict possible future evolution of S. glossinidius in the context of genome reduction. Finally, knockout simulations in different metabolic systems reveal a gradual decrease in network robustness to different mutational events for bacterial endosymbionts at different stages of the symbiotic association.ConclusionsStoichiometric analysis reveals few gene inactivation events whose effects on the functionality of S. glossinidius metabolic systems are drastic enough to account for the ecological transition from a free-living to host-dependent lifestyle. The decrease in network robustness across different metabolic systems may be associated with the progressive integration in the more stable environment provided by the insect host. Finally, reductive evolution simulations reveal the strong influence that external conditions exert on the evolvability of metabolic systems.
Highlights
Genome reduction is a common evolutionary process observed in bacterial lineages that have established associations, both symbiotic and pathogenic, with eukaryotic hosts
Gene deletion events had been restricted to those genes presents in closer relative enterobacterial genomes and for which the genomic context is extensively conserved between S. glossinidius and E. coli K12, in order to exclude deleted genes originated by horizontal gene transfer events that may not be functional in the ancestor
The reconstruction and functional analysis of the S. glossinidius metabolic network at different stages of the genome reduction process reveal how this evolutionary process affects the overall functionality of this bacterium in the context of its association with the tsetse host
Summary
Genome reduction is a common evolutionary process observed in bacterial lineages that have established associations, both symbiotic and pathogenic, with eukaryotic hosts. There is a massive proliferation of different types of mobile genetic elements in these initial stages of genome reduction, representing an important source of genome rearrangements [5,6] This gene inactivation process is enhanced by drastic reduction in the effective population size of these bacterial endosymbionts (i.e. population bottlenecks associated to their strict vertical transmission from mothers to offspring), allowing the accumulation of slight deleterious mutations by random genetic drift in a process known as Muller’s ratchet [7]. Genome reduction is studied from a systems biology perspective through the reconstruction and functional analysis of genome-scale metabolic networks of S. glossinidius
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