Production of Current by Syntrophy Between Exoelectrogenic and Fermentative Hyperthermophilic Microorganisms in Heterotrophic Biofilm from a Deep-Sea Hydrothermal Chimney

Abstract

To study the role of exoelectrogens within the trophic network of deep-sea hydrothermal vents, we performed successive subcultures of a hyperthermophilic community from a hydrothermal chimney sample on a mix of electron donors in a microbial fuel cell system. Electrode (the electron acceptor) was swapped every week to enable fresh development from spent media as inoculum. The MFC at 80 °C yielded maximum current production increasing from 159 to 247 mA m−2 over the subcultures. The experiments demonstrated direct production of electric current from acetate, pyruvate, and H2 and indirect production from yeast extract and peptone through the production of H2 and acetate from fermentation. The microorganisms found in on-electrode communities were mainly affiliated to exoelectrogenic Archaeoglobales and Thermococcales species, whereas in liquid media, the communities were mainly affiliated to fermentative Bacillales and Thermococcales species. The work shows interactions between fermentative microorganisms degrading complex organic matter into fermentation products that are then used by exoelectrogenic microorganisms oxidizing these reduced compounds while respiring on a conductive support. The results confirmed that with carbon cycling, the syntrophic relations between fermentative microorganisms and exoelectrogens could enable some microbes to survive as biofilm in extremely unstable conditions.

Schematic representation of cross-feeding between fermentative and exoelectrogenic microbes on the surface of the conductive support. B, Bacillus/Geobacillus spp.; Tc, Thermococcales; Gg, Geoglobus spp.; Py, pyruvate; Ac, acetate.

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Acknowledgments

The authors thank Erwan Roussel (LM2E, IFREMER Brest) for helpful suggestions, Céline Rommevaux and Françoise Lesongeur for sampling during the MOMARSAT 2014 cruise, the MIM platform (MIO, France) for providing access to their confocal microscopy facility, and the GeT-PlaGe platform (GenoToul, France) for DNA sequencing.

Funding

This work received financial support from the CNRS national interdisciplinary research program (PEPS-ExoMod 2016). The project leading to this publication has received funding from European FEDER program under project 1166-39417.

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Correspondence to Pierre-Pol Liebgott.

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Pillot, G., Davidson, S., Auria, R. et al. Production of Current by Syntrophy Between Exoelectrogenic and Fermentative Hyperthermophilic Microorganisms in Heterotrophic Biofilm from a Deep-Sea Hydrothermal Chimney. Microb Ecol 79, 38–49 (2020). https://doi.org/10.1007/s00248-019-01381-z

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Keywords

  • Electromicrobiology
  • Exoelectrogenic
  • Hyperthermophilic microorganisms
  • Microbial interaction
  • Deep-sea hydrothermal vent