Interspecies interactions mediated by conductive minerals in the sediments of the iron rich meromictic Lake La Cruz, Spain

Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. Here we show that conductive particles drove the metabolic coupling between electroactive microbial clades from this environment. The anoxic sediment of Lake La Cruz was rich in biogeochemically ‘reactive’ iron minerals, and harbored known electroactive species such as Geobacter and Methanothrix, in addition to groups not ever linked to an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed 2 to 4 times higher methanogenic activity, as compared to incubations with non-conductive glass beads or without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated above 8 mM depending on substrate (8 ± 0.6 to 11.7 ± 1.2 mM). Only by enabling syntrophic acetate oxidation with conductive minerals we could prevent acetate accumulation. Acetate oxidation conductively coupled to methanogenic activity had a stoichiometric recovery of 70% and could be maintained in subsequent transfers if and only if amended with conductive particles. Mud-free enrichments without conductive particles ceased any metabolic activity after the second transfer. Conductive particles preserved a consortium of Youngiibacter-Methanothrix, whereas without conductive particles Youngiibacter spp. died off. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles inferring that minerals may have arbitrated the earliest interspecies associations