Abstract
Tor Caldara is a shallow-water gas vent located in the Mediterranean Sea, with active venting of CO2 and H2S. At Tor Caldara, filamentous microbial biofilms, mainly composed of Epsilon- and Gammaproteobacteria, grow on substrates exposed to the gas venting. In this study, we took a metaproteogenomic approach to identify the metabolic potential and in situ expression of central metabolic pathways at two stages of biofilm maturation. Our findings indicate that inorganic reduced sulfur species are the main electron donors and CO2 the main carbon source for the filamentous biofilms, which conserve energy by oxygen and nitrate respiration, fix dinitrogen gas and detoxify heavy metals. Three metagenome-assembled genomes (MAGs), representative of key members in the biofilm community, were also recovered. Metaproteomic data show that metabolically active chemoautotrophic sulfide-oxidizing members of the Epsilonproteobacteria dominated the young microbial biofilms, while Gammaproteobacteria become prevalent in the established community. The co-expression of different pathways for sulfide oxidation by these two classes of bacteria suggests exposure to different sulfide concentrations within the biofilms, as well as fine-tuned adaptations of the enzymatic complexes. Taken together, our findings demonstrate a shift in the taxonomic composition and associated metabolic activity of these biofilms in the course of the colonization process.
Highlights
Marine gas vents transport volatile elements and compounds from the geosphere to the hydrosphere by seepage through sediments and bedrocks (Suess, 2014)
The EF biofilm was dominated by Gammaproteobacteria (54%), followed by Epsilonproteobacteria (29%) and small proportions of Bacteroidia (4%) and Alphaproteobacteria (3%; Figure 1A)
A reverse trend was observed in the YF biofilm, with Epsilonproteobacteria (67%) dominating the community, followed by Gammaproteobacteria (23%), Bacteroidia (2%), and Alphaproteobacteria (1%; Figure 1A)
Summary
Marine gas vents transport volatile elements and compounds from the geosphere to the hydrosphere by seepage through sediments and bedrocks (Suess, 2014). At these sites, geological processes, biogeochemical reactions and the activity of microorganisms act together to alter the composition of volatile products. Shallowwater hydrothermal and gas vents are associated with submarine volcanoes, arc and back-arc volcanoes and occur globally in the proximity of active plate margins and intraplate hotspots (reviewed in Price and Giovannelli, 2017). Volcanic arc hydrothermal systems release large volumes of volatiles, because of both degassing of the subducted slab and the mantle, and the decomposition of carbonates in the overlying marine sediments (Barry et al, 2019). Since most of the known venting in the Mediterranean is from shallow vents, the majority of the outlets are of the gasohydrothermal type, emitting large volumes of carbon dioxide
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