Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase

Abstract

Background: The ars gene system provides arsenic resistance for a variety of microorganisms and can be chromosomal or plasmid-borne. The arsC gene, which codes for an arsenate reductase is essential for arsenate resistance and transforms arsenate into arsenite, which is extruded from the cell. A survey of GenBank shows that arsC appears to be phylogenetically widespread both in organisms with known arsenic resistance and those organisms that have been sequenced as part of whole genome projects.

Results: Phylogenetic analysis of aligned arsC sequences shows broad similarities to the established 16S rRNA phylogeny, with separation of bacterial, archaeal, and subsequently eukaryotic arsC genes. However, inconsistencies between arsC and 16S rRNA are apparent for some taxa. Cyanobacteria and some of the gamma-Proteobacteria appear to possess arsC genes that are similar to those of Low GC Gram-positive Bacteria, and other isolated taxa possess arsC genes that would not be expected based on known evolutionary relationships. There is no clear separation of plasmid-borne and chromosomal arsC genes, although a number of the Enterobacteriales (gamma-Proteobacteria) possess similar plasmid-encoded arsC sequences.

Conclusion: The overall phylogeny of the arsenate reductases suggests a single, early origin of the arsC gene and subsequent sequence divergence to give the distinct arsC classes that exist today. Discrepancies between 16S rRNA and arsC phylogenies support the role of horizontal gene transfer (HGT) in the evolution of arsenate reductases, with a number of instances of HGT early in bacterial arsC evolution. Plasmid-borne arsC genes are not monophyletic suggesting multiple cases of chromosomal-plasmid exchange and subsequent HGT. Overall, arsC phylogeny is complex and is likely the result of a number of evolutionary mechanisms.

Figure 1

Phylogenetic tree based on 16S rRNA gene sequences.The tree was constructed by neighbor joining methods using 1326 informative positions. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. The names of the major divisions of prokaryotes represented are shown to the right of corresponding clades.

Figure 2

Evolutionary distance tree based on arsC gene sequences. The tree was constructed by neighbor joining methods using 408 informative positions. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. Plasmid-borne arsC genes are indicated by "plasmid" following the organism name. Names in boxes represent branches that are inconsistent with the 16S rRNA tree.

Figure 3

Maximum parsimony tree based on arsC gene sequences.The tree was constructed using the same 408 informative positions used in the ED analysis. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. Plasmid-borne arsC genes are indicated by "plasmid" following the organism name. Names in boxes represent branches that are inconsistent with the 16S rRNA tree.