Hyperexpansion of genetic diversity and metabolic capacity of extremophilic bacteria and archaea in ancient Andean Lake sediments

Abstract

Abstract Background: The Andean Altiplano hosts a repertoire of high-altitude lakes with harsh conditions for life. These lakes are undergoing a process of desiccation caused by the current climate, leaving terraces exposed to extreme atmospheric conditions and serving as analogs to Martian paleolake basins. Microbiomes in Altiplano lake terraces have been poorly studied, enclosing uncultured lineages and a great opportunity to understand environmental adaptation and the limits of life on Earth. Here we examine the microbial diversity and function in ancient sediments (10.3-11 ky BP (Before Present)) from a terrace profile of Laguna Lejía, a sulfur- and metal/metalloid-rich saline lake in the Chilean Altiplano. We also evaluate the physical and chemical changes of the lake over time by studying the mineralogy and geochemistry of the terrace profile. Results: The mineralogy and geochemistry of the terrace profile revealed large water level fluctuations in the lake, scarcity of organic carbon, and high concentration of SO43--S, Na, Cl and Mg. Lipid biomarker analysis indicated the presence of aquatic/terrestrial plant remnants preserved in the ancient sediments, and genome-resolved metagenomics unveiled a diverse prokaryotic community with still active microorganisms based on in silico growth predictions. We reconstructed 591 bacterial and archaeal metagenome-assembled genomes (MAGs), of which 98.8% belonged to previously unreported species. The most abundant and widespread metabolisms among MAGs were the reduction and oxidation of S, N, As and halogenated compounds, as well as CO oxidation, possibly as a key metabolic trait in the organic carbon-depleted sediments. The broad redox and CO2 fixation pathways among phylogenetically distant bacteria and archaea extended the knowledge of metabolic capacities to previously unknown taxa. For instance, we identified genomic potential for dissimilatory sulfate reduction in Bacteroidota and α- and γ-Proteobacteria; ammonium oxidation in a novel Actinobacteriota; and we predicted enzymes of the Calvin-Benson-Bassham cycle in Planctomycetota, Gemmatimonadota, and Nanoarchaeota. The presence of genes encoding for enzymes involved in the above metabolic pathways in unexpected taxonomic groups has significant implications for the expansion of microorganisms involved in the biogeochemical cycles of carbon, nitrogen and sulfur.