Enzyme phylogenies as markers for the oxidation state of the environment: The case of respiratory arsenate reductase and related enzymes

Abstract

BackgroundPhylogenies of certain bioenergetic enzymes have proved to be useful tools for deducing evolutionary ancestry of bioenergetic pathways and their relationship to geochemical parameters of the environment. Our previous phylogenetic analysis of arsenite oxidase, the molybdopterin enzyme responsible for the biological oxidation of arsenite to arsenate, indicated its probable emergence prior to the Archaea/Bacteria split more than 3 billion years ago, in line with the geochemical fact that arsenite was present in biological habitats on the early Earth. Respiratory arsenate reductase (Arr), another molybdopterin enzyme involved in microbial arsenic metabolism, serves as terminal oxidase, and is thus situated at the opposite end of bioenergetic electron transfer chains as compared to arsenite oxidase. The evolutionary history of the Arr-enzyme has not been studied in detail so far.ResultsWe performed a genomic search of genes related to arrA coding for the molybdopterin subunit. The multiple alignment of the retrieved sequences served to reconstruct a neighbor-joining phylogeny of Arr and closely related enzymes. Our analysis confirmed the previously proposed proximity of Arr to the cluster of polysulfide/thiosulfate reductases but also unravels a hitherto unrecognized clade even more closely related to Arr. The obtained phylogeny strongly suggests that Arr originated after the Bacteria/Archaea divergence in the domain Bacteria, and was subsequently laterally distributed within this domain. It further more indicates that, as a result of accumulation of arsenate in the environment, an enzyme related to polysulfide reductase and not to arsenite oxidase has evolved into Arr.ConclusionThese findings are paleogeochemically rationalized by the fact that the accumulation of arsenate over arsenite required the increase in oxidation state of the environment brought about by oxygenic photosynthesis.

Metagenomic study of red biofilms from Diamante Lake reveals ancient arsenic bioenergetics in haloarchaea

“…However, the low boostrapping support for the position of haloarchaea clade within the Firmicutes lineage makes this concept a speculation at this point. The ArrA phylogenetic tree does not resemble the evolutionary history of the bacterial lineages carrying ArrA enzymes and suggests that multiple horizontal gene transfer events might have taken place in the past, as it was also proposed previously (Duval et al, 2008). Nevertheless, our analyses indicate that most likely haloarchaea ArrA enzymes were obtained in one single (and ancient) event in the past, probably when arsenic-rich environments were more common scenarios on Earth.…”

“…As a positive control for our phylogenetic analyses, we used the 107 CISM/DMSO protein sequences alignment published by Duval et al (2008). We identically reproduced their results using Neighbor joining (NJ), Poisson model, 500 bootstrap repetitions and uniform rates.…”

“…Members of both Bacteria and Archaea encode aio genes for As(III) oxidation, which could be used for chemolithotrophic growth (van Lis et al, 2013). Some Bacteria have also genes for dissimilatory arsenate (As(V)) reduction (arr genes), associated to anaerobic respiration using arsenate as terminal electron acceptor (Duval et al, 2008). It has been proposed that anaerobic arsenate respiration is a more recent metabolism than arsenite oxidation, emerged once oxygen became abundant at the atmosphere (van Lis et al, 2013).…”

Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon

“…Concatenated sequences of core subunits of these operons have a strong similarity, suggesting recent duplication events that led to their formation. Phylogenetic analysis of catalytic molybdenum subunits placed HSR2 polysulfide reductases in a distinct haloarchaea-specific cluster, adjacent to the Psr/Phs family (Duval et al, 2008) (Figure 4, Supplementary Figure S6). Catalytic subunit A phylogeny and core genes organization attribute a fourth operon of molybdopterin oxidoreductase to the clade of tetrathionate reductases.…”

“…Thus, the above SreA was added manually along with its top 10 UniProtKB hits. The homologous sequences were included to the previous dataset (Duval et al, 2008) after removal of partial sequences (ArrA_DesDC; ArrA_DesY5; ArrA_SulBa; ArrA_BacSe; Psr/PhsA_ DesDe; AroA_AlcFa). Upon manual removal of duplicates, the final dataset consisted of 147 sequences.…”