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

Thermodynamic models predict that H is energetically favorable for seafloor microbial life, but how H affects anabolic processes in seafloor-associated communities is poorly understood. Here, we used quantitative C DNA stable isotope probing (qSIP) to quantify the effect of H on carbon assimilation by microbial taxa synthesizing C-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, peridotite-associated taxa increased assimilation of C-bicarbonate and C-acetate into 16S rRNA genes of operational taxonomic units by 146% (±29%) and 55% (±34%), respectively, which correlated with enrichment of H-oxidizing NiFe-hydrogenases encoded in peridotite-associated metagenomes. The effect of H on anabolism was phylogenetically organized, with taxa affiliated with Atribacteria, Nitrospira, and Thaumarchaeota exhibiting the most significant increases in C-substrate assimilation in the presence of H. In SIP incubations with added H, an order of magnitude higher number of peridotite rock-associated taxa assimilated C-bicarbonate, C-acetate, and C-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-metabolizing, rock-associated taxa that can increase anabolism under high H concentrations. Because ultramafic rocks are widespread in slow-, and ultraslow-spreading oceanic lithosphere, continental margins, and subduction zones where H is formed in copious amounts, the link between H and carbon assimilation demonstrated here may be widespread within these geological settings.