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

Ömer K. Coskun, Aurèle Vuillemin, Florence Schubotz, Frieder Klein, Susanna E. Sichel, Wolfgang Eisenreich & William D. Orsi

The ISME Journal https://doi.org/10.1038/s41396-021-01066-x

Abstract

Thermodynamic models predict that H₂ is energetically favorable for seafloor microbial life, but how H₂ affects anabolic processes in seafloor-associated communities is poorly understood. Here, we used quantitative ¹³C DNA stable isotope probing (qSIP) to quantify the effect of H₂ on carbon assimilation by microbial taxa synthesizing ¹³C-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 H₂, peridotite-associated taxa increased assimilation of ¹³C-bicarbonate and ¹³C-acetate into 16S rRNA genes of operational taxonomic units by 146% (±29%) and 55% (±34%), respectively, which correlated with enrichment of H₂-oxidizing NiFe-hydrogenases encoded in peridotite-associated metagenomes. The effect of H₂ on anabolism was phylogenetically organized, with taxa affiliated with Atribacteria, Nitrospira, and Thaumarchaeota exhibiting the most significant increases in ¹³C-substrate assimilation in the presence of H₂. In SIP incubations with added H2, an order of magnitude higher number of peridotite rock-associated taxa assimilated ¹³C-bicarbonate, ¹³C-acetate, and ¹³C-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 H2-metabolizing, rock-associated taxa that can increase anabolism under high H₂ concentrations. Because ultramafic rocks are widespread in slow-, and ultraslow-spreading oceanic lithosphere, continental margins, and subduction zones where H₂ is formed in copious amounts, the link between H₂ and carbon assimilation demonstrated here may be widespread within these geological settings.