Novel Barite Chimneys at the Loki's Castle Vent Field Shed Light on Key Factors Shaping Microbial Communities and Functions in Hydrothermal Systems

In order to fully understand the cycling of elements in hydrothermal systems it is critical to understand intra-field variations in geochemical and microbiological processes in both focused, high-temperature and diffuse, low-temperature areas. To reveal important causes and effects of this variation, we performed an extensive chemical and microbiological characterization of a low-temperature venting area in the Loki's Castle Vent Field (LCVF). This area, located at the flank of the large sulfide mound, is characterized by numerous chimney-like barite (BaSO4) structures (≤ 1 m high) covered with white cotton-like microbial mats. Results from geochemical analyses, microscopy (FISH, SEM), 16S rRNA gene amplicon-sequencing and metatranscriptomics were compared to results from previous analyses of biofilms growing on black smoker chimneys at LCVF. Based on our results, we constructed a conceptual model involving the geochemistry and microbiology in the LCVF. The model suggests that CH4 and H2S are important electron donors for microorganisms in both high-temperature and low-temperature areas, whereas the utilization of H2 seems restricted to high-temperature areas. This further implies that sub-seafloor processes can affect energy-landscapes, elemental cycling, and the metabolic activity of primary producers on the seafloor. In the cotton-like microbial mats on top of the active barite chimneys, a unique network of single cells of Epsilonproteobacteria interconnected by threads of extracellular polymeric substances (EPS) was seen, differing significantly from the long filamentous Sulfurovum filaments observed in biofilms on the black smokers. This network also induced nucleation of barite crystals and is suggested to play an essential role in the formation of the microbial mats and the chimneys. Furthermore, it illustrates variations in how different genera of Epsilonproteobacteria colonize and position cells in different vent fluid mixing zones within a vent field. This may be related to niche-specific physical characteristics. Altogether, the model provides a reference for future studies and illustrates the importance of systematic comparative studies of spatially closely connected niches in order to fully understand the geomicrobiology of hydrothermal systems.