Molecular hydrogen is an overlooked energy source for marine bacteria

Abstract

Molecular hydrogen (H2) and carbon monoxide (CO) are supersaturated in seawater relative to the atmosphere and hence are readily accessible energy sources for marine microbial communities. Yet while marine CO oxidation is well-described, it is unknown whether seawater communities consume H2. Here we integrated genome-resolved metagenomics, biogeochemistry, thermodynamic modelling, and culture-based analysis to profile H2 and CO oxidation by marine bacteria. Based on analysis of 14 surface water samples, collected from three locations spanning tropical to subantarctic fronts, three uptake hydrogenase classes are prevalent in seawater and encoded by major marine families such as Rhodobacteraceae, Flavobacteriaceae, and Sphingomonadaceae. However, they are less abundant and widespread than carbon monoxide dehydrogenases. Consistently, microbial communities in surface waters slowly consumed H2 and rapidly consumed CO at environmentally relevant concentrations, with H2 oxidation most active in subantarctic waters. The cell-specific power from these processes exceed bacterial maintenance requirements and, for H2, can likely sustain growth of bacteria with low energy requirements. Concordantly, we show that the polar ultramicrobacterium Sphingopyxis alaskensis grows mixotrophically on H2 by expressing a group 2a [NiFe]-hydrogenase, providing the first demonstration of atmospheric H2 oxidation by a marine bacterium. Based on TARA Oceans metagenomes, genes for trace gas oxidation are globally distributed and are fourfold more abundant in deep compared to surface waters, highlighting that trace gases are important energy sources especially in energy-limited waters. Altogether, these findings show H2 is a significant energy source for marine communities and suggest that trace gases influence the ecology and biogeochemistry of oceans globally.