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

Microbial communities inhabiting extreme environments like Salar de Huasco (SH) are adapted to thrive while exposed to several abiotic pressures and the presence of toxic elements like arsenic (As). Hence, we aimed to uncover the role of arsenic 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 arsenic (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 showed broadly convergent patterns, contrasting with their great taxonomic variability. Arsenic-related metabolism is different among the five communities, as well as other functional categories like those related to the CH4 and S cycles. Particularly, we found that the distribution and abundance of As-related genes increase, following along the As concentration gradient. Approximately 75% of the detected genes for As-metabolism belong to expulsion mechanisms, being arsJ and arsP pumps related to sites with higher As concentrations and present almost exclusively in Proteobacteria. Furthermore, taxonomic diversity and functional potential are reflected in the 12 reconstructed high-quality MAGs (Metagenome Assembled Genomes) belonging to the Bacteroidetes (5), Proteobacteria (5), Cyanobacteria (1) and Gemmatimonadota (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 the highly toxic As. Finally, this environment represents a reservoir of unknown and undescribed microorganisms, with a great metabolic versatility, which needs further study. IMPORTANCEMicrobial communities inhabiting extreme environments are fundamental for maintaining the ecosystems; however, little is known about their potential functions and interactions among them. We sampled the microbial communities in Salar de Huasco (SH) in the Chilean Altiplano, a fragile and complex environment that comprises several stresses. We found that microbes in SH are taxonomically diverse; nonetheless, their functional potential seems to have an important convergence degree, suggesting high adaptation levels. Particularly, arsenic metabolism showed differences associated with increasing concentrations of the metalloid throughout the area, and it is effectively exerting a clear and significant pressure over these organisms. Thus, this researchs significance is that we described highly specialized communities thriving in little-explored environments under several pressures, considered analogous of early Earth and other planets, and can have the potential for unraveling technologies to face climate change repercussions in many areas of interest.