Evolution of Thermophilic Microbial Communities from a Deep-Sea Hydrothermal Chimney under Electrolithoautotrophic Conditions with Nitrate

Abstract

Recent studies have shown the presence of an abiotic electrical current across the walls of deep-sea hydrothermal chimneys, allowing the growth of electroautotrophic microbial communities. To understand the role of the different phylogenetic groups and metabolisms involved, this study focused on electrotrophic enrichment with nitrate as electron acceptor. The biofilm density, community composition, production of organic compounds, and electrical consumption were monitored by FISH confocal microscopy, qPCR, metabarcoding, NMR, and potentiostat measurements. A statistical analysis by PCA showed the correlation between the different parameters (qPCR, organic compounds, and electron acceptors) in three distinct temporal phases. In our conditions, the Archaeoglobales have been shown to play a key role in the development of the community as the first colonizers on the cathode and the first producers of organic compounds, which are then used as an organic source by heterotrophs. Finally, through subcultures of the community, we showed the development of a greater biodiversity over time. This observed phenomenon could explain the biodiversity development in hydrothermal contexts, where energy sources are transient and unstable.

Spark of Life: Role of electrotrophy in the emergence of Life

“…With the recent discovery of electrical currents within deep-sea hydrothermal vents [14], a new potential energy source has been identified. As previously mentioned, recent studies have demonstrated the ability of modern electrotrophs from hydrothermal vents to grow from an external electric current, coupled with the fixation of CO2 and the reduction of different electron acceptor, such as nitrate, sulfate, CO2, O2 and iron-oxide [28][29][30]. Based on these observations, we can assume that Life have evolved to use an electrical current in combination with a range of different electron acceptors.…”

“…In recent studies, the ability of some microorganisms from modern hydrothermal vents to grow using only electricity as an energy source has been demonstrated, either focusing on hyperthermophiles [28][29][30], or in-situ using electrical current generated from the hydrothermal fluid [31]. This metabolism was defined as a new trophic type, as compared to photo-or chemo-trophy, named electrotrophy [32].…”

“…Once an energetic system has been set up within the proto-cell, it is now necessary to focus on the proto-system of CO2 fixation into more complex organic molecules. Most electrotrophs enriched on cathodes fix CO2 through the reductive acetyl-CoA, also called Wood-Ljungdhal (WL), autotrophic pathway [29,39]. This autotrophic pathway is arguably considered to be the oldest pathway, whose genes were present in LUCA [57] because it is the least energy intensive (1 mole of ATP per mol of CO2).…”

“…Previous experiments have indicated that under conditions mimicking hydrothermal vents, electric current could have a direct effect on this pathway in Archaeoglobales [29]. Indeed, the constant influx of electrons into the cell causes an overactivity of this CO2 assimilation pathway, through the rapid and continuous turnover of reduced ferredoxins, leading to the accumulation of pyruvate in the medium.…”

Electron transfer of extremophiles in bioelectrochemical systems

“…Still, multiple lines of evidence suggest geothermal electricity generation in deep hydrothermal systems. Nevertheless, so far we do not have characterized isolates from these field sites but Pillot et al could at least show enrichment data for cathodic growth of inocula taken at a deep-sea hydrothermal chimney (Nakamura et al 2010 ; Pillot et al 2021 ). Nevertheless, a direct interaction of isolated extremophiic microorganisms with cathodes has some biotechnological potential as it could offer the possibility to use autotrophic organisms and an electrical current as starting points for a carbon dioxide-based biotechnology.…”