Abstract
The hypersaline lagoon system of Araruama (HLSA) is one of the largest in the world and one of the most important sources of evaporative salt in Brazil. The biogeochemical characteristics of this lagoon system led it to be considered a Precambrian relic. The HLSA also harbors extensive microbial mats, but the taxonomic and metabolic attributes of these mats are poorly understood. Our high-throughput metagenomics analyses demonstrated that the HLSA microbial mats are dominated by Proteobacteria, Cyanobacteria, and Bacteroidetes. Among Proteobacteria, Deltaproteobacteria comprises approximately 40% of the total population and it includes sulfate-reducing bacteria such as Desulfobacterales, Desulfuromonadales, and Desulfovibrionales. Differing in composition and function of their reaction centers, other phylogenetic diverse anoxygenic phototrophic bacteria were detected in the HLSA microbial mats metagenomes. The presence of photolithoautotrophs, sulfate reducers, sulfide oxidizers, and aerobic heterotrophs suggests the existence of numerous cooperative niches that are coupled and regulated by microbial interactions. We suggest that the HLSA microbial mats hold microorganisms and the necessary machinery (genomic repertoire to sustain metabolic pathways) to promote favorable conditions (i.e., create an alkaline pH microenvironment) for microbially mediated calcium carbonate precipitation process. Metagenome-assembled genomes (Ca. Thiohalocapsa araruaensisHLSAbin6 sp. nov. andCa. Araruabacter turfaeHLSAbin9 gen. nov. sp. nov.) obtained support the relevance of Sulfur metabolism and they are enriched with genes involved in the osmoadaptive networks, hinting at possible strategies to withstand osmotic stress. Metabolically versatile bacteria populations, able to use multiple nutrient sources and osmolytes, seem to be a relevant attribute to survive under such stressful conditions.
Highlights
Microbial mats are one of the oldest known ecosystems on Earth
This study aimed at gaining insights into the diversity of microorganisms in the hypersaline lagoon system of Araruama (HLSA) microbial mats, expanding the knowledge generated by previous studies that employed operational taxonomic unit-based approach to focus on the cyanobacterial populations of these microbial mats (Ramos et al, 2017), and the prokaryotic diversity of the HLSA water column (Clementino et al, 2008)
Hypersaline lagoon system of Araruama microbial mats have evolved to encompass high taxonomic and metabolic diversity, illustrated by the autotrophic and heterotrophic guilds found in their metagenomes
Summary
Microbial mats are one of the oldest known ecosystems on Earth. They support complex consortia of many interdependent species belonging to different functional groups (van Gemerden, 1993; Bolhuis et al, 2014). Exopolymeric substances (EPSs) excreted by these complex microbial communities protect them against environmental stressors such as desiccation and excessive light These substances represent an important source of Organic Carbon under oligotrophic conditions and can serve as nucleation centers for carbonate precipitation processes (Rossi and De Philippis, 2015; Cangemi et al, 2016). These characteristics allow microbial mats to thrive in a variety of harsh environments around the world including hypersaline ecosystems, where intense evaporation and low levels of freshwater input lead to high salt concentrations in the water
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