Abstract
Deep-sea hydrothermal vents are extreme and complex ecosystems based on a trophic chain. We are still unsure of the identities of the first colonizers of these environments and their metabolism, but they are thought to be (hyper)thermophilic autotrophs. Here we investigate whether the electric potential observed across hydrothermal chimneys could serve as an energy source for these first colonizers. Experiments were performed in a two-chamber microbial electrochemical system inoculated with deep-sea hydrothermal chimney samples, with a cathode as sole electron donor, CO2 as sole carbon source, and nitrate, sulfate, or oxygen as electron acceptors. After a few days of culturing, all three experiments showed growth of electrotrophic biofilms consuming the electrons (directly or indirectly) and producing organic compounds including acetate, glycerol, and pyruvate. Within the biofilms, the only known autotroph species retrieved were members of Archaeoglobales. Various heterotrophic phyla also grew through trophic interactions, with Thermococcales growing in all three experiments as well as other bacterial groups specific to each electron acceptor. This electrotrophic metabolism as energy source driving initial microbial colonization of conductive hydrothermal chimneys is discussed.
Highlights
Deep-sea hydrothermal vents are extreme and complex ecosystems based on a trophic chain
Recent studies have shown the exoelectrogenic ability of some hyperthermophilic microorganisms isolated from deepsea hydrothermal vents belonging to Archaeoglobales and Thermococcales[11,12,13], but no studies have been done on environmental samples potentially harboring electrotrophic communities growing naturally with an electric current as their sole energy source
The electrode potential has been chosen in order to prevent the abiotic cathodic reduction of the culture medium (Supplementary Fig. S1), the electrode was poised at − 590 mV/SHE in the presence of sulfate and nitrate as electron acceptors while this potential was − 300 mV/SHE in the presence of oxygen as electron acceptor
Summary
Deep-sea hydrothermal vents are extreme and complex ecosystems based on a trophic chain. Various heterotrophic phyla grew through trophic interactions, with Thermococcales growing in all three experiments as well as other bacterial groups specific to each electron acceptor This electrotrophic metabolism as energy source driving initial microbial colonization of conductive hydrothermal chimneys is discussed. Isolated in the deep ocean, far away from sunlight and subsequent organic substrates, the primary energy sources for the development of this abundant biosphere remain elusive in these extreme, mineral-rich environments Since their discovery, many new metabolisms have been identified based on organic or inorganic molecules. Recent studies have shown the exoelectrogenic ability of some hyperthermophilic microorganisms isolated from deepsea hydrothermal vents belonging to Archaeoglobales and Thermococcales[11,12,13], but no studies have been done on environmental samples potentially harboring electrotrophic communities growing naturally with an electric current as their sole energy source
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