A Unique Natural Laboratory to Study Polyextremophile Microorganisms: Diamante Lake as a Window to the Origin of Life

Abstract

Diamante Lake is located at 4589 m above sea level (m a.s.l.) inside the Galán Volcano caldera and presents extreme environmental conditions, such as high arsenic concentration (210 mg l-1), salinity, pH and UV radiation. Until 2010, most studies in the area had largely overlooked the microbial biodiversity in Diamante Lake. With the advent of high throughput sequencing, it became possible to study the microbial communities of environmental samples using metagenomic approaches. In a recent work, we discovered red biofilms forming on the surface of sedimentary rocks on the bottom of the lake containing the rare mineral gaylussite. A metagenomic analysis of these biofilms revealed a predominance of haloarchaea (>96%) over other prokaryotic or eukaryotic organisms. To thrive under the extreme conditions in the lake, these biofilms use different metabolic and physiologic strategies: (1) to avoid the arsenic uptake into the cell, this is done through highly specific phosphate transporters (Pst) and consequently, (2) to take advantage bioenergetically of the high extracellular arsenic concentration and obtain energy from arsenite oxidation and to perform anaerobic respiration of arsenate. Contrary to what could be expected, the required enzymes for these arsenic metabolisms were likely not acquired recently by the selective pressure within Diamante Lake, but rather correspond to reminiscences of primitive metabolisms that could date back to even the origins of the haloarchaea lineage billions of years ago. Diamante Lake is a unique environment in the world and represents an open window to study the evolution of life on Earth and the adaptations required to survive under the extreme conditions that prevailed on the ancient Earth and that are currently found on other planets.