Genomics-based insights into the expanded diversity and adaptation strategies of hadal trench anammox bacteria

Abstract Anaerobic ammonium oxidation (anammox) bacteria are an important functional guild in the nitrogen cycle and contribute up to 50% of nitrogen loss in the global ocean. Hadal trenches have been recognized as a hotspot of marine biogeochemical cycles; however, the metabolic traits, ecological adaptations, and potential origins of anammox bacteria in this critical habitat remain largely unexplored. Here, we reconstructed eight anammox metagenome-assembled genomes from sediments of four hadal trenches (Diamantina, Kermadec, Mariana, and Yap), which represent four out of the five distinct anammox bacterial families (i.e. Candidatus Scalinduaceae, Ca. Anammoxibacteraceae, Ca. Subterrananammoxibiaceae, and Ca. Bathyanammoxibiaceae). The dominant trench anammox bacteria, affiliated with Ca. Scalindua, were similar to those found in shallow coastal sediments and oxygen-deficient seawaters. Beyond the core anammox metabolism, the hadal Ca. Scalindua genomes contain genes encoding cyanase and urease, indicating that they can utilize cyanate and urea besides ammonium to thrive in the hadal trenches. Compared to trench-derived Ca. Subterrananammoxibiaceae and Ca. Bathyanammoxibiaceae, ABC-type Fe3+ transporter and sulfate transporter CysZ could help trench-derived Ca. Anammoxibacteraceae genomes to uptake Fe3+ and synthesize sulfur-containing amino acids. Molecular clock analysis suggests that the ancestors of the hadal anammox bacterial lineages appeared on Earth 1.46–0.07 billion years ago, significantly earlier than the geological formation of the trenches. The first hadal anammox bacteria were likely derived from shallower sediments and were transported into the trenches via sediment wasting. Overall, our study reveals a remarkable diversity of hadal anammox bacteria and their origin as well as survival strategies in hadal sediments.