Hydrogen-dependent dissimilatory nitrate reduction to ammonium enables growth of Campylobacterota isolates

Abstract

Dissimilatory nitrate reduction to ammonium (DNRA) is a key process in global nitrogen cycling, supporting the energy conservation of diverse microbes. For a long time, DNRA has been thought to primarily depend on organic electron donors, and thus to be governed by carbon-to-nitrogen (C:N) ratios. However, recent studies suggest that inorganic electron donors, such as sulfur compounds and iron, may also facilitate DNRA. The coupling of DNRA with molecular hydrogen (H2) oxidation is theoretically feasible, but largely unexplored microbial process. Here, we report the isolation of two Campylobacterota strains, Aliarcobacter butzleri hDNRA1 and Sulfurospirillum sp. hDNRA2, that grow by using H2 as an electron donor for DNRA. In both batch and continuous cultures, DNRA sensu stricto, i.e., NO2--to-NH + reduction, depended on the presence of H2 and was stoichiometric with H2 oxidation. The electrons for NO - reduction were clearly derived from H, and hydrogenotrophic DNRA was largely unaffected by the ratio of either carbon or electron donor to NO -/NO -. Genomic and transcriptomic analyses indicate that group 1b [NiFe]-hydrogenase and cytochrome c552 nitrite reductase are the key enzymes catalyzing hydrogenotrophic DNRA. These findings reveal novel physiological mechanisms enabling anaerobic bacterial growth, challenge the traditional C:N ratio paradigm, and uncover new biogeochemical processes and mediators controlling the global nitrogen and hydrogen cycles.