Abstract
BackgroundPerchlorate is a widely distributed anion that is toxic to humans, but serves as a valuable electron acceptor for several lineages of bacteria. The ability to utilize perchlorate is conferred by a horizontally transferred piece of DNA called the perchlorate reduction genomic island (PRI).MethodsWe compared genomes of perchlorate reducers using phylogenomics, SNP mapping, and differences in genomic architecture to interrogate the evolutionary history of perchlorate respiration.ResultsHere we report on the PRI of 13 genomes of perchlorate-reducing bacteria from four different classes of Phylum Proteobacteria (the Alpha-, Beta-, Gamma- and Epsilonproteobacteria). Among the different phylogenetic classes, the island varies considerably in genetic content as well as in its putative mechanism and location of integration. However, the islands of the densely sampled genera Azospira and Magnetospirillum have striking nucleotide identity despite divergent genomes, implying horizontal transfer and positive selection within narrow phylogenetic taxa. We also assess the phylogenetic origin of accessory genes in the various incarnations of the island, which can be traced to chromosomal paralogs from phylogenetically similar organisms.ConclusionThese observations suggest a complex phylogenetic history where the island is rarely transferred at the class level but undergoes frequent and continuous transfer within narrow phylogenetic groups. This restricted transfer is seen directly by the independent integration of near-identical islands within a genus and indirectly due to the acquisition of lineage-specific accessory genes. The genomic reversibility of perchlorate reduction may present a unique equilibrium for a metabolism that confers a competitive advantage only in the presence of an electron acceptor, which although widely distributed, is generally present at low concentrations in nature.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2011-5) contains supplementary material, which is available to authorized users.
Highlights
Perchlorate is a widely distributed anion that is toxic to humans, but serves as a valuable electron acceptor for several lineages of bacteria
Perchlorate/chlorate reducers are restricted to certain subclades within the Proteobacteria All of the genomes used in this study are publically available and their accession numbers along with associated references for their phenotypic descriptions are provided in Additional file 2: Table S1
To assess the phylogenetic relationships between dissimilatory perchloratereducing bacteria (DPRB) and other bacteria, we adopted a multi-locus sequence analysis (MLSA) method that relies upon an in-house pipeline for identifying as many orthologs as possible within a given group of bacteria
Summary
Perchlorate is a widely distributed anion that is toxic to humans, but serves as a valuable electron acceptor for several lineages of bacteria. Since our original identification of the PRI, we have accumulated 9 additional genome sequences of DPRB, including isolates from the Epsilon- and Gammaproteobacteria [5, 6]. We sought to identify mechanisms of integration and excision of the PRI, in addition to uncovering the evolutionary history of the individual genes in the PRI. In answering these questions, we made observations about the evolution of the PRI that led us to propose new explanations for the origin, evolution, and ecological significance of bacterial perchlorate respiration
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