Microbial mats, microbialites and endoevaporites in High Andean Wetlands: A source of biodiversity and alternative geochemical cycles

Abstract

Andean Wetlands are extreme environments where microbial ecosystems develop inassociation with minerals, either precipitating (e.g., carbonates), or finding shelter (e.g.,gypsum, halite). These ecosystems in which microbes associate with minerals (MAM)include biofilms, microbial mats, microbialites and endoevaporites.Here we present the first report of a wide diversity of MAM ecosystems found in Andeanwetlands. They include mats and endoevaporitic systems associated with gypsum and halite(in Tebenquiche), mats, carbonates microbialites and ¨phytomicrobialites¨ (in La Brava),stromatolites (in Socompa) and biofilms associated with gaylussite in Laguna Diamante(inside Volcano Galan). All of these MAM are high productive systems developing undermultiple-extreme conditions. Oxygen and sulfide profiles indicated the presence of variousmetabolisms, but not that of oxygenic photosynthesis, as the main autotrophic process insome of these MAM. Microbial diversity demonstrated to be very different to previouslystudied MAM ecosystems across the world: MAM in Atacama, Chile, were dominated byArchaea (Crenearcheota and Euryarcheota), Planctomycetes and OP1 group. Cyanobacteriaand Proteobacteria were almost absent; therefore suggesting that oxygenic and anoxygenicphotosynthesis are not the dominant carbon fixation process. This raises the question howthese ecosystems fix carbon and obtain energy? We speculate that the answer lies inalternative carbon fixation pathways described for Creanearchaeota, Plantomycetes andOP1, metagenomic analyses of alternative carbon fixation pathways are presented. Inaddition, the relationship between arsenic and Archaea: based on arsenite oxidase andarsenate reductase are presented. This is based on metagenomic studies performed redbiofilm that flourish associated to gaylussite in the bottom of microbialites in LakeDiamante (Volcano Galan at 4650 m altitude), under extreme conditions such as higharsenic concentration, alkalinity, salinity and UV radiation and low oxygen. These biofilmsare composed of Haloarchaea (93%) (16S rRNA shotgun sequencing). Metagenomicanalysis indicated a high abundance of arsenite oxidases (Aio) and respiratory arsenate(As(V)) reductases (ArrA) encoded by the Haloarchaea. Phylogenetic analysis revealed anew clade of Aio enzymes in this group of Archaea that gives stronger support to theLUCA hypothesis. A pure culture of an Halorubrum strain isolated from the biofilm,showed the presence of Aio and ArrA genes, and enhanced growth in presence of As(III)under both light and dark conditions with an effective oxidation of As(III) to As(V),indicating that Aio enzymes are functional.