Phosphate-Arsenic Interactions in Halophilic Microorganisms of the Microbial Mat from Laguna Tebenquiche: from the Microenvironment to the Genomes

Abstract

Arsenic (As) is a metalloid present in the earth’s crust and widely distributed in the environment. Due to its high concentrations in the Andean valleys and its chemical similarity with phosphorus (P), its biological role in Andean Microbial Ecosystems (AMEs) has begun to be studied. The AMEs are home to extremophilic microbial communities that form microbial mats, evaporites, and microbialites inhabiting Andean lakes, puquios, or salt flats. In this work, we characterize the biological role of As and the effect of phosphate in AMEs from the Laguna Tebenquiche (Atacama Desert, Chile). Using micro X-ray fluorescence, the distribution of As in microbial mat samples was mapped. Taxonomic and inferred functional profiles were obtained from enriched cultures of microbial mats incubated under As stress and different phosphate conditions. Additionally, representative microorganisms highly resistant to As and able to grow under low phosphate concentration were isolated and studied physiologically. Finally, the genomes of the isolated Salicola sp. and Halorubrum sp. were sequenced to analyze genes related to both phosphate metabolism and As resistance. The results revealed As as a key component of the microbial mat ecosystem: (i) As was distributed across all sections of the microbial mat and represented a significant weight percentage of the mat (0.17 %) in comparison with P (0.40%); (ii) Low phosphate concentration drastically changed the microbial community in microbial mat samples incubated under high salinity and high As concentrations; (iii) Archaea and Bacteria isolated from the microbial mat were highly resistant to arsenate (up to 500 mM), even under low phosphate concentration; (iv) The genomes of the two isolates were predicted to contain key genes in As metabolism (aioAB and arsC/acr3) and the genes predicted to encode the phosphate-specific transport operon (pstSCAB-phoU) are next to the arsC gene, suggesting a functional relationship between these two elements.