Thriving of hyperthermophilic microbial communities from a deep-sea sulfidic hydrothermal chimney under electrolithoautotrophic conditions with nitrate as electron acceptor

Pillot, Guillaume; Davidson, Sylvain; Shintu, Laetitia; Tanet, Lisa; Combet-Blanc, Yannick; Godfroy, Anne; Bonin, Patricia; Liebgott, Pierre-Pol

doi:10.1101/2021.03.26.437165

Cited by 4 publications

(1 citation statement)

References 59 publications

(66 reference statements)

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“…Given these elements, the identified Archaeoglobales species could be, under our electrolithoautotrophic conditions, the first colonizers of the electrode during the first days of growth. This hypothesis was confirmed into a more detailed study focusing on the enrichment on nitrate 21 .…”

Section: Discussionmentioning

confidence: 60%

Identification of enriched hyperthermophilic microbial communities from a deep-sea hydrothermal vent chimney under electrolithoautotrophic culture conditions

Pillot

Ali

Davidson

et al. 2021

Sci Rep

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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.

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Section: Discussionmentioning

confidence: 60%

Identification of enriched hyperthermophilic microbial communities from a deep-sea hydrothermal vent chimney under electrolithoautotrophic culture conditions

Pillot

Ali

Davidson

et al. 2021

Sci Rep

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Optimization of growth and electrosynthesis of PolyHydroxyAlcanoates by the thermophilic bacterium Kyrpidia spormannii

PILLOT

Sunny

Comes

et al. 2021

Preprint

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The electrosynthesis of valuable compounds by biofilms on electrodes is being intensively studied since few years. However, so far, the actual biofilms growing on cathodes produce mainly small and relatively inexpensive compounds such as acetate or ethanol. Recently, a novel Knallgas bacterium, Kyrpidia spormannii EA-1 has been described to grow on cathodes under thermophilic and microaerophilic conditions, producing significant amounts of PolyHydroxyAlkanoates (PHAs). These PHA are promising sustainable bioplastic polymers with the potential to replace petroleum-derived plastics in a variety of applications. However, the effect of culture conditions and electrode properties on the growth of K. spormannii EA-1 biofilms and PHA production is still unclear. In this study, we report on the optimization of growth and PHA production in liquid culture and on the cathode of a Microbial Electrosynthesis System. Optimization of the preculture allows to obtain high cell density of up to 8.5 Log10 cells·ml-1 in 48h, decreasing the time necessary by a factor of 2.5. With respect to cathodic biofilm formation, this study was focused on the optimization of three main operating parameters, which are the applied cathode potential, buffer pH, and the oxygen concentration in the feed gas. Maximum biofilm formation and PHA production was observed at an applied potential of -844mV vs. SCE, pH 6.5, O2 saturation of 2.5%. The PHA concentration in the biofilm reached a maximum of ≈26.8 μg·cm-2 after optimization, but at 2.9% the coulombic efficiency remains relatively low. We expect that further nutrient limitation will allow the accumulation of more PHA, based on a dense biofilm growth. In conclusion, these findings take microbial electrosynthesis of PHA a step forward towards practical implementation.

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Spark of Life: Role of Electrotrophy in the Emergence of Life

Pillot

Santiago

Kerzenmacher

et al. 2023

Life

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The emergence of life has been a subject of intensive research for decades. Different approaches and different environmental “cradles” have been studied, from space to the deep sea. Since the recent discovery of a natural electrical current through deep-sea hydrothermal vents, a new energy source is considered for the transition from inorganic to organic. This energy source (electron donor) is used by modern microorganisms via a new trophic type, called electrotrophy. In this review, we draw a parallel between this metabolism and a new theory for the emergence of life based on this electrical electron flow. Each step of the creation of life is revised in the new light of this prebiotic electrochemical context, going from the evaluation of similar electrical current during the Hadean, the CO2 electroreduction into a prebiotic primordial soup, the production of proto-membranes, the energetic system inspired of the nitrate reduction, the proton gradient, and the transition to a planktonic proto-cell. Finally, this theory is compared to the two other theories in hydrothermal context to assess its relevance and overcome the limitations of each. Many critical factors that were limiting each theory can be overcome given the effect of electrochemical reactions and the environmental changes produced.

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Thriving of hyperthermophilic microbial communities from a deep-sea sulfidic hydrothermal chimney under electrolithoautotrophic conditions with nitrate as electron acceptor

Cited by 4 publications

References 59 publications

Identification of enriched hyperthermophilic microbial communities from a deep-sea hydrothermal vent chimney under electrolithoautotrophic culture conditions

Identification of enriched hyperthermophilic microbial communities from a deep-sea hydrothermal vent chimney under electrolithoautotrophic culture conditions

Optimization of growth and electrosynthesis of PolyHydroxyAlcanoates by the thermophilic bacterium Kyrpidia spormannii

Spark of Life: Role of Electrotrophy in the Emergence of Life

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