Quantifying the effects of hydrogen on carbon assimilation in a seafloor microbial community associated with ultramafic rocks

Thermodynamic models predict that H-2 is energetically favorable for seafloor microbial life, but how H-2 affects anabolic processes in seafloor-associated communities is poorly understood. Here, we used quantitative C-13 DNA stable isotope probing (qSIP) to quantify the effect of H-2 on carbon assimilation by microbial taxa synthesizing C-13-labeled DNA that are associated with partially serpentinized peridotite rocks from the equatorial Mid-Atlantic Ridge. The rock-hosted seafloor community was an order of magnitude more diverse compared to the seawater community directly above the rocks. With added H-2, peridotite-associated taxa increased assimilation of C-13-bicarbonate and C-13-acetate into 16S rRNA genes of operational taxonomic units by 146% (+/- 29%) and 55% (+/- 34%), respectively, which correlated with enrichment of H-2-oxidizing NiFe-hydrogenases encoded in peridotite-associated metagenomes. The effect of H-2 on anabolism was phylogenetically organized, with taxa affiliated with Atribacteria, Nitrospira, and Thaumarchaeota exhibiting the most significant increases in C-13-substrate assimilation in the presence of H-2. In SIP incubations with added H-2, an order of magnitude higher number of peridotite rock-associated taxa assimilated C-13-bicarbonate, C-13-acetate, and C-13-formate compared to taxa that were not associated with peridotites. Collectively, these findings indicate that the unique geochemical nature of the peridotite-hosted ecosystem has selected for H-2-metabolizing, rock-associated taxa that can increase anabolism under high H-2 concentrations. Because ultramafic rocks are widespread in slow-, and ultraslow-spreading oceanic lithosphere, continental margins, and subduction zones where H-2 is formed in copious amounts, the link between H-2 and carbon assimilation demonstrated here may be widespread within these geological settings.