Microbial diversity, metabolic specialization, and genomic novelty across polyextreme saline lakes of the Central Dry Andes

The high-altitude saline lakes of the Central Dry Andes are polyextreme environments characterized by hypersalinity, high alkalinity, fluctuating redox conditions, and elevated levels of trace metals (e.g., Li, As, Mn, Mg). These conditions challenge microbial life yet select for highly specialized and functionally versatile communities. Through metagenomic analyses across four lakes (Colorada, Hedionda, Mama Khumu, and Loromayu), we identified taxonomic assemblages dominated by halophilic and halotolerant bacteria (e.g., Halomonas, Marinobacter, Rhodohalobacter), phototrophic cyanobacteria and algae (Dunaliella, Chlorella), archaeal Halobacteria (Halorubrum, Natrinema, Haloterrigena), and halotolerant fungi (Aspergillus, Penicillium). Notably, Laguna Mama Khumu exhibited the highest microbial and functional diversity, reflecting its heterogeneous salinity and richer chemical gradients, whereas the most extreme lakes (Colorada and Loromayu) harbored narrower specialized communities. Across all sites, oxidative phosphorylation dominated as the primary metabolic strategy. Additional pathways such as photosynthesis, sulfur and methane cycling were especially prominent at Mama Khumu. Patterns of carbohydrate-active enzyme (CAZyme) also diverged: Loromayu harbored abundant glycoside hydrolases, indicating strong polysaccharide degradation potential, while Mama Khumu displayed a boarder and more functionally redundant CAZyme repertoire. High-quality metagenome-assembled genomes (MAGs) uncovered novel lineages (< 95% ANI to known species) encoding key traits including energy metabolism (ATP synthase, anoxygenic photosynthesis), sulfur oxidation, arsenic resistance, and heavy-metal efflux systems. These features highlight the genomic innovation fostered by polyextreme conditions. Overall, our findings showed that within a shared scaffold of aerobic respiration and halophilic resilience, local geochemistry drives divergent taxonomic and metabolic adaptations. The Bolivian Andean saline lakes thus emerge as natural laboratories for studying microbial adaptation under multiple stressors and offer promising sources for biotechnological discovery.