Phylogenetic Structure and Metabolic Properties of Microbial Communities in Arsenic-Rich Waters of Geothermal Origin

Arsenic (As) is a toxic element released in aquatic environments by geogenic processes or anthropic activities. To counteract its toxicity, several microorganisms have developed mechanisms to tolerate and utilize it for respiratory metabolism. However, still little is known about identity and physiological properties of microorganisms exposed to natural high levels of As and the role they play in As transformation and mobilization processes. This work aims to explore the phylogenetic composition and functional properties of aquatic microbial communities in As-rich freshwater environments of geothermal origin and to elucidate the key microbial functional groups that directly or indirectly may influence As-transformations across a natural range of geogenic arsenic contamination. Distinct bacterial communities in terms of composition and metabolisms were found. Members of Proteobacteria, affiliated to Alpha- and Betaproteobacteria were mainly retrieved in groundwaters and surface waters, whereas Gammaproteobacteria were the main component in thermal waters. Most of the OTUs from thermal waters were only distantly related to 16S rRNA gene sequences of known taxa, indicating the occurrence of bacterial biodiversity so far unexplored. Nitrate and sulfate reduction and heterotrophic As(III)-oxidization were found as main metabolic traits of the microbial cultivable fraction in such environments. No growth of autotrophic As(III)-oxidizers, autotrophic and heterotrophic As(V)-reducers, Fe-reducers and oxidizers, Mn-reducers and sulfide oxidizers was observed. The ars genes, involved in As(V) detoxifying reduction, were found in all samples whereas aioA [As(III) oxidase] and arrA genes [As(V) respiratory reductase] were not found. Overall, we found that As detoxification processes prevailed over As metabolic processes, concomitantly with the intriguing occurrence of novel thermophiles able to tolerate high levels of As.