Abstract
BackgroundGenome reduction is a common evolutionary process in symbiotic and pathogenic bacteria. This process has been extensively characterized in bacterial endosymbionts of insects, where primary mutualistic bacteria represent the most extreme cases of genome reduction consequence of a massive process of gene inactivation and loss during their evolution from free-living ancestors. Sodalis glossinidius, the secondary endosymbiont of tsetse flies, contains one of the few complete genomes of bacteria at the very beginning of the symbiotic association, allowing to evaluate the relative impact of mobile genetic element proliferation and gene inactivation over the structure and functional capabilities of this bacterial endosymbiont during the transition to a host dependent lifestyle.ResultsA detailed characterization of mobile genetic elements and pseudogenes reveals a massive presence of different types of prophage elements together with five different families of IS elements that have proliferated across the genome of Sodalis glossinidius at different levels. In addition, a detailed survey of intergenic regions allowed the characterization of 1501 pseudogenes, a much higher number than the 972 pseudogenes described in the original annotation. Pseudogene structure reveals a minor impact of mobile genetic element proliferation in the process of gene inactivation, with most of pseudogenes originated by multiple frameshift mutations and premature stop codons. The comparison of metabolic profiles of Sodalis glossinidius and tsetse fly primary endosymbiont Wiglesworthia glossinidia based on their whole gene and pseudogene repertoires revealed a novel case of pathway inactivation, the arginine biosynthesis, in Sodalis glossinidius together with a possible case of metabolic complementation with Wigglesworthia glossinidia for thiamine biosynthesis.ConclusionsThe complete re-analysis of the genome sequence of Sodalis glossinidius reveals novel insights in the evolutionary transition from a free-living ancestor to a host-dependent lifestyle, with a massive proliferation of mobile genetic elements mainly of phage origin although with minor impact in the process of gene inactivation that is taking place in this bacterial genome. The metabolic analysis of the whole endosymbiotic consortia of tsetse flies have revealed a possible phenomenon of metabolic complementation between primary and secondary endosymbionts that can contribute to explain the co-existence of both bacterial endosymbionts in the context of the tsetse host.
Highlights
Genome reduction is a common evolutionary process in symbiotic and pathogenic bacteria
Fourth, during the re-annotation process we detected 142 situations in which a putative functional gene had been split in an ORF included in the primary annotation as a functional gene and a pseudogene detected in our FASTA and BLASTP searches
These pseudogenes were eliminated from the final re-annotation file and a “misc_feature” qualifier were added to the corresponding functional genes specifying the proportion of the ancestral gene represented by the originally annotated gene and the characterized pseudogene
Summary
Genome reduction is a common evolutionary process in symbiotic and pathogenic bacteria This process has been extensively characterized in bacterial endosymbionts of insects, where primary mutualistic bacteria represent the most extreme cases of genome reduction consequence of a massive process of gene inactivation and loss during their evolution from free-living ancestors. Based on the evolutionary age of the symbiotic association and the extent of codependence between both symbiotic partners, bacterial endosymbionts are classified into primary and secondary. The former are generally essential for their hosts, reside exclusively inside specialized host cells called bacteriocytes, are transmitted by strict vertical transmission from mother to descendents and the associations with their insect hosts are usually ancient. The strict vertical transmission from mothers to descendents leads to the coevolution between the bacterial endosymbionts and their hosts [19,20,21]
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