Desulfatiglans-related bacteria associated with conductive mineral particles in marine subsurface sediments

Acetate is a key intermediate in anaerobic mineralization of organic matter in marine sediments. Recent observations suggest that acetate is oxidized syntrophically in the methanic zone of marine sediments, and that electrically conductive mineral particles could provide niches for electroactive microbial communities that perform this process. We combined radiotracer measurements, a novel procedure for ferromagnetic mineral particle extraction, and metagenomic analyses to examine this process in Baltic Sea sediments. Our results confirm that acetate is oxidized syntrophically across and below the sulfate-methane transition zones of the sediments, where the transfer of reducing equivalents from acetate oxidation to CO₂ fuels methanogenesis. Ferromagnetic particles consistently occurred throughout the geochemical zones and mainly consisted of the electrically conductive minerals magnetite and pyrite-greigite. The microbial communities associated with ferromagnetic particles were dominated by members phylogenetically affiliated with the bacterial genus Desulfatiglans. Known Desulfatiglans species are dissimilatory sulfate reducers; however, metagenome-assembled genomes indicate that Desulfatiglandales populations associated with ferromagnetic particles lack genetic potential to respire sulfate. Instead, they may grow by acetate oxidation coupled with extracellular electron transfer, consistent with a conductive mineral-associated lifestyle. We hypothesize that Desulfatiglans relatives are acetate-oxidizing partners in a syntrophic process facilitated by interspecies electron transfer via conductive particles. We identified cytochrome-rich ANME-1 archaea as the predominant methane-cycling microorganisms associated with ferromagnetic particles; however, their potential role as methanogenic syntrophic partners remains uncertain. Overall, our study reveals that distinct microbial communities are associated with ferromagnetic particles and shows conductive minerals as a niche for electroactive microorganisms in marine sediments.

Acetate is a central intermediate in the anaerobic breakdown of organic matter. In Baltic Sea sediments at and below the sulfate-methane transition zone, we observed acetate oxidation to carbon dioxide at rates similar to methane formation from carbon dioxide reduction, a pattern indicative of syntrophic acetate oxidation. Previous enrichment studies suggest that electrically conductive mineral surfaces can facilitate this process. Motivated by this observation, we extracted ferromagnetic conductive particles from sediments and compared particle-attached microbial communities with bulk sediment. Particle-attached communities were distinct and enriched in the bacterial genus Desulfatiglans. Their genomes lacked genes for sulfate respiration, yet encoded traits consistent with acetate oxidation and extracellular electron transfer. Our findings suggest conductive minerals as distinct microbial niches and highlight Desulfatiglans-related bacteria as a potential key organism in particle-associated acetate oxidation.