Living to the High Extreme: Unraveling the Composition, Structure, and Functional Insights of Bacterial Communities Thriving in the Arsenic-Rich Salar de Huasco Altiplanic Ecosystem

Abstract

ABSTRACT Microbial communities inhabiting extreme environments such as Salar de Huasco (SH) in northern Chile are adapted to thrive while exposed to several abiotic pressures and the presence of toxic elements such as arsenic (As). Hence, we aimed to uncover the role of As in shaping bacterial composition, structure, and functional potential in five different sites in this altiplanic wetland using a shotgun metagenomic approach. The sites exhibit wide gradients of As (9 to 321 mg/kg), and our results showed highly diverse communities and a clear dominance exerted by the Proteobacteria and Bacteroidetes phyla. Functional potential analyses show broadly convergent patterns, contrasting with their great taxonomic variability. As-related metabolism, as well as other functional categories such as those related to the CH4 and S cycles, differs among the five communities. Particularly, we found that the distribution and abundance of As-related genes increase as the As concentration rises. Approximately 75% of the detected genes for As metabolism belong to expulsion mechanisms; arsJ and arsP pumps are related to sites with higher As concentrations and are present almost exclusively in Proteobacteria. Furthermore, taxonomic diversity and functional potential are reflected in the 12 reconstructed high-quality metagenome assembled genomes (MAGs) belonging to the Bacteroidetes (5), Proteobacteria (5), Cyanobacteria (1), and Gemmatimonadetes (1) phyla. We conclude that SH microbial communities are diverse and possess a broad genetic repertoire to thrive under extreme conditions, including increasing concentrations of highly toxic As. Finally, this environment represents a reservoir of unknown and undescribed microorganisms, with great metabolic versatility, which needs further study. IMPORTANCE As microbial communities inhabiting extreme environments are fundamental for maintaining ecosystems, many studies concerning composition, functionality, and interactions have been carried out. However, much is still unknown. Here, we sampled microbial communities in the Salar de Huasco, an extreme environment subjected to several abiotic stresses (high UV radiation, salinity and arsenic; low pressure and temperatures). We found that although microbes are taxonomically diverse, functional potential seems to have an important degree of convergence, suggesting high levels of adaptation. Particularly, arsenic metabolism showed differences associated with increasing concentrations of the metalloid throughout the area, and it effectively exerts a significant pressure over these organisms. Thus, the significance of this research is that we describe highly specialized communities thriving in little-explored environments subjected to several pressures, considered analogous of early Earth and other planets, that have the potential for unraveling technologies to face the repercussions of climate change in many areas of interest.

Keywords

• extremophiles
• metagenomics
• arsenic
• MAGs
• altiplano