Conductive Particles Enable Syntrophic Acetate Oxidation between Geobacter and Methanosarcina from Coastal Sediments

Coastal sediments are rich in conductive minerals, which could impact microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure and their survival depends on successful partnership. Here we demonstrate that conductive minerals facilitate a SAO partnership between Geobacter and Methanosarcina from the coastal sediments of the Bothnian Bay, Baltic Sea. Bothnian methanogenic sediments showed a high apparent isotopic fractionation (αc 1.07) characteristic of CO2-reductive methanogenesis. The native community was represented by electrogens such as Geobacter and methanogens like Methanosarcina. Upon the addition of conductive particles (activated carbon and magnetite), methanogenesis from acetate increased fourfold. Geobacter (96% related to G. psychrophilus) and Methanosarcina (99% related to M. subterranea) dominated the conductive particle-spiked SAO communities. Using NanoSIMS we demonstrated that during SAO, Geobacter incorporated 82% of the labeled acetate as compared to only 18% by Methanosarcina. At the same time, Geobacter converted 27% of the 13C-acetate to 13CO2 as detected by IRMS. Indigenous soluble shuttles were not involved in SAO, since spiking fresh cultures with spent-media filtrate had no effect on methanogenic rates. Our results demonstrate that Geobacter oxidizes acetate to CO2 while transferring electrons extracellularly via conductive particles to Methanosarcina, which utilizes them for CO2 reduction to methane. In natural environments, mediation of SAO by conductive particles between electrogens and methanogens could impact the iron and methane cycles.