From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources

Abstract

At deep-sea vent systems, hydrothermal emissions rich in reductive chemicals replace solar energy as fuels to support microbial carbon assimilation. Until recently, all the microbial components at vent systems have been assumed to be fostered by the primary production of chemolithoautotrophs; however, both the laboratory and on-site studies demonstrated electrical current generation at vent systems and have suggested that a portion of microbial carbon assimilation is stimulated by the direct uptake of electrons from electrically conductive minerals. Here we show that chemolithoautotrophic Fe(II)-oxidizing bacterium, Acidithiobacillus ferrooxidans, switches the electron source for carbon assimilation from diffusible Fe2+ ions to an electrode under the condition that electrical current is the only source of energy and electrons. Site-specific marking of a cytochrome aa3 complex (aa3 complex) and a cytochrome bc1 complex (bc1 complex) in viable cells demonstrated that the electrons taken directly from an electrode are used for O2 reduction via a down-hill pathway, which generates proton motive force that is used for pushing the electrons to NAD+ through a bc1 complex. Activation of carbon dioxide fixation by a direct electron uptake was also confirmed by the clear potential dependency of cell growth. These results reveal a previously unknown bioenergetic versatility of Fe(II)-oxidizing bacteria to use solid electron sources and will help with understanding carbon assimilation of microbial components living in electronically conductive chimney habitats.

Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “CandidatusTenderia electrophaga”

“…During growth under standard culture conditions, the acidophilic iron oxidizer A. ferrooxidans is predicted to have a ratio closer to 90/10% for the forward versus reverse pathways, including the proton gradient necessary to generate ATP (36). Recent experimental evidence suggests that the ratio of electron utilization by the forward and reverse pathways during growth on an electrode is close to 15:1 in A. ferrooxidans (15). …”

“…Electroautotrophic growth is assumed for MCL based on an increase in biomass correlated to increasing current, a lack of organic carbon in the bioelectrochemical reactor, and identification of an active Calvin-Benson-Bassham (CBB) cycle (13). Electroautotrophic growth of isolates at potentials greater than −100 mV versus the standard hydrogen electrode (SHE) has thus far been demonstrated only for the aerobic Fe(II)-oxidizing bacteria Mariprofundus ferrooxydans PV-1 and Acidithiobacillus ferrooxidans (14, 15), while other autotrophs require supplemental energy from light or hydrogen for initial growth on a cathode (6, 16). However, recent reports indicate that communities enriched on high potential O 2 -reducing biocathodes reproducibly contain large populations of Gammaproteobacteria (17, 18).…”

‘Candidatus Tenderia electrophaga', an uncultivated electroautotroph from a biocathode enrichment

“…Several isolates have been obtained from aerobic biocathodes, but none are autotrophic, despite the evidence that autotrophy is possible . Attempts to grow autotrophic bacteria in pure cultures on high potential [>À0.1 V vs Standard Hydrogen Electrode (SHE)] electrodes have had limited success, including very slow growth and limited production of biomass (Bose et al, 2014;Ishii et al, 2015;Summers et al, 2013).…”

Extracellular Electron Transfer of <i>Pseudomonas stutzeri</i> Driven by Lithotrophic and Mixotrophic Denitrification

“…The lack of OM cytochromes is in harmony with the inability of P. stutzeri to extract electron directly from an electrode (trace 2, Fig. 2), and this aspect is in sharp contrast with Fe-oxidizing bacteria such as Acidithiobacillus ferrooxidans 17 and Mariprofundus ferrooxidans 18 which exploits OM cytochromes as the primal conduit for EET to/from electrodes.…”