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Carbon and Arsenic Metabolism in Thiomonas Strains: Differences Revealed Diverse Adaptation Processes

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Carbon and Arsenic Metabolism in Thiomonas Strains: Differences Revealed Diverse Adaptation Processes

Christopher G Bryan et al. BMC Microbiol.

Abstract

Background: 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. 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.

Results: The 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.

Conclusion: Taken 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.

Figures

Figure 1
Figure 1
Phylogenetic dendrogram of the SuperGene construct of both the 16S rRNA and rpoA genes (A) of the Thiomonas strains used in this study. Ralstonia eutropha H16 served as the outgroup. Numbers at the branches indicate percentage bootstrap support from 500 re-samplings for ML analysis. NJ analyses (not shown) produced the same branch positions in each case. The scale bar represents changes per nucleotide. (B) Phylogenetic dendrogram of the arsB genes of the Thiomonas strains used in this study and some other closely-related bacteria. Both ML and NJ (not shown) analysis gave the same tree structure. The scale bar represents changes per nucleotide. Sequences obtained using the arsB1- and arsB2-specific internal primers were not included in the analysis as the sequences produced were of only between 200 – 350 nt in length.
Figure 2
Figure 2
Carbon fixed as a product of As(III) oxidised by T. arsenivorans. Error bars, where visible, show standard deviation; n = 3 for each data point.
Figure 3
Figure 3
Differential proteomic analysis in T. arsenivorans and Thiomonas sp. 3As strains, in response to As(III). On the gel presented are extracts obtained from (A) T. arsenivorans or (B)Thiomonas sp. 3As cultivated in the absence (left) or in the presence (right) of 2.7 mM As(III). Spots that are circled showed significant differences of accumulation pattern when the two growth conditions were compared. Protein sizes were evaluated by comparison with protein size standards (BenchMark™ Protein Ladder, Invitrogen).

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