Carbon and arsenic metabolism in Thiomonas strains: differences revealed diverse adaptation processes

Christopher G Bryan,Christelle Lemaitre-Guillier,Fabienne Battaglia-Brunet,Didier Lièvremont,Florence Arsène-Ploetze,Marie Marchal,Valérie Kugler,Philippe N Bertin

doi:10.1186/1471-2180-9-127

Abstract

BackgroundThiomonas strains are ubiquitous in arsenic-contaminated environments. Differences between Thiomonas strains in the way they have adapted and respond to arsenic have never been studied in detail. For this purpose, five Thiomonas strains, that are interesting in terms of arsenic metabolism were selected: T. arsenivorans, Thiomonas spp. WJ68 and 3As are able to oxidise As(III), while Thiomonas sp. Ynys1 and T. perometabolis are not. Moreover, T. arsenivorans and 3As present interesting physiological traits, in particular that these strains are able to use As(III) as an electron donor.ResultsThe metabolism of carbon and arsenic was compared in the five Thiomonas strains belonging to two distinct phylogenetic groups. Greater physiological differences were found between these strains than might have been suggested by 16S rRNA/rpoA gene phylogeny, especially regarding arsenic metabolism. Physiologically, T. perometabolis and Ynys1 were unable to oxidise As(III) and were less arsenic-resistant than the other strains. Genetically, they appeared to lack the aox arsenic-oxidising genes and carried only a single ars arsenic resistance operon. Thiomonas arsenivorans belonged to a distinct phylogenetic group and increased its autotrophic metabolism when arsenic concentration increased. Differential proteomic analysis revealed that in T. arsenivorans, the rbc/cbb genes involved in the assimilation of inorganic carbon were induced in the presence of arsenic, whereas these genes were repressed in Thiomonas sp. 3As.ConclusionTaken together, these results show that these closely related bacteria differ substantially in their response to arsenic, amongst other factors, and suggest different relationships between carbon assimilation and arsenic metabolism.

Highlights

Thiomonas strains are ubiquitous in arsenic-contaminated environments
In agreement with previous data, strains 3As, WJ68 and T. arsenivorans oxidised arsenite to arsenate in liquid media whereas T. perometabolis and Ynys1 did not (Table 1)
In the presence of arsenic, T. arsenivorans is still able to express proteins required for optimal growth whereas 3As is not. These observations revealed that carbon assimilation, energy acquisition and arsenic metabolism of these strains are linked

Summary

Introduction

Thiomonas strains are ubiquitous in arsenic-contaminated environments. Differences between Thiomonas strains in the way they have adapted and respond to arsenic have never been studied in detail. A major anthropogenic source is the mining industry, where the processing of sulfide ores produces large quantities of sulfidic wastes which may be rich in arsenic-bearing compounds such as arsenopyrite The weathering of these minerals leads to the formation of acid mine drainage (AMD), generally characterised by elevated sulfate, iron and other metal concentrations [2], and the transport of many toxic elements such as inorganic forms of arsenic, arsenite (As(III)) and arsenate (As(V)). This often results in chronic and severe pollution of the surrounding environment, with a substantial reduction of the indigenous biota

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