Bacterial chemolithoautotrophy in ultramafic plumes along the Mid-Atlantic Ridge

Hydrothermal vent systems release reduced chemical compounds that act as an important energy source in the deep sea. Chemolithoautotrophic microbes inhabiting hydrothermal plumes oxidize these compounds, in particular, hydrogen and reduced sulfur, to obtain the energy required for CO2 fixation. Here, we analysed the planktonic communities of four hydrothermal systems located along the Mid-Atlantic Ridge: Irinovskoe, Semenov-2, Logatchev-1, and Ashadze-2, by combining long-read 16S rRNA gene analysis, fluorescence in situ hybridization, meta-omics, and thermodynamic calculations. Sulfurimonas and SUP05 dominated the microbial communities in these hydrothermal plumes. Investigation of Sulfurimonas and SUP05 MAGs, and their gene transcription in plumes indicated a niche partitioning driven by hydrogen and sulfur. In addition to sulfur and hydrogen oxidation, a novel SAR202 clade inhabiting the plume, here referred to as genus Carboxydicoccus, harbours the capability for CO oxidation and CO2 fixation via reverse TCA cycle. Both pathways were also highly transcribed in other hydrogen-rich plumes, including the Von Damm vent field. Carboxydicoccus profundi reached up to 4% relative abundance (1.0 x 103 cell ml- 1) in Irinovskoe non-buoyant plume and was also abundant in non-hydrothermally influenced deep-sea metagenomes (up to 5 RPKM). Therefore, CO, which is probably not sourced from the hydrothermal fluids (1.9-5.8 μM), but rather from biological activities within the rising fluid, may serve as a significant energy source in hydrothermal plumes. Taken together, this study sheds light on the chemolithoautotrophic potential of the bacterial community in Mid-Atlantic Ridge plumes.