Candidatus Hydrothermarchaeota, formally called Marine Benthic Group E, has often been detected in iron-and sulfur-rich marine environments, such as hydrothermal vents and cold seeps. However, their ecology and physiology remain unclear. Cultivated representatives of this group are still lacking and only several metagenome-assembled genomes (MAGs) and single-amplified genomes (SAGs) are available from two deep-sea hydrothermal areas, the Juan de Fuca Ridge (JdFR) and Guaymas Basin (GB), in the northeast Pacific. We herein report four MAGs of Ca. Hydrothermarchaeota recovered from hydrothermally-inactive metal sulfide deposits at the Southern Mariana Trough (SMT) in the northwest Pacific. A phylogenetic analysis indicated that the MAGs of the SMT were distinct from those of the JdFR and GB at the genus or potentially family level. Ca. Hydrothermarchaeota MAGs from the SMT commonly possessed putative genes for carboxydotrophic and hydrogenotrophic respiration using oxidized chemical species of sulfur as electron acceptors and also for carbon fixation, as reported previously in MAGs/SAGs from the JdFR and GB. This result strongly supports Ca. Hydrothermarchaeota containing anaerobic chemolithoautotrophs using carbon monoxide and/or hydrogen as electron donors. A comparative genome analysis highlighted differences in the capability of nitrogen fixation between MAGs from the SMT and the other fields, which are consistent with environmental differences in the availability of nitrogen sources for assimilation between the fields. Based on the wide distribution in various areas, abundance, and metabolic potential of Ca. Hydrothermarchaeota, they may play a role in the biogeochemical cycling of carbon, nitrogen, sulfur, and iron in marine environments, particularly in deep-sea hydrothermal fields.

Magnetosome-producing microorganisms can sense and move toward the redox gradient and have been extensively studied in terrestrial and shallow marine sediment environments. However, given the difficulty of sampling, magnetotactic bacteria (MTB) are poorly explored in deep-sea hydrothermal fields. In this study, a deep-sea hydrothermal vent chimney from the Southern Mariana Trough was collected using a remotely operated submersible. The mineralogical and geochemical characterization of the vent chimney sample showed an internal iron redox gradient. Additionally, the electron microscopy of particles collected by magnetic separation from the chimney sample revealed MTB cells with bullet-shaped magnetosomes, and there were minor occurrences of cuboctahedral and hexagonal prismatic magnetosomes. Genome-resolved metagenomic analysis was performed to identify microorganisms that formed magnetosomes. A metagenome-assembled genome (MAG) affiliated with Nitrospinae had magnetosome genes such as mamA, mamI, mamM, mamP, and mamQ. Furthermore, a diagnostic feature of MTB genomes, such as magnetosome gene clusters (MGCs), including mamA, mamP, and mamQ, was also confirmed in the Nitrospinae-affiliated MAG. Two lines of evidence support the occurrence of MTB in a deep-sea, inactive hydrothermal vent environment.