Comparative single-cell genomics of Atribacterota JS1 in the Japan Trench hadal sedimentary biosphere.

Deep-sea and subseafloor sedimentary environments host heterotrophic microbial communities that contribute to Earth's carbon cycling. However, the potential metabolic functions of individual microorganisms and their biogeographical distributions in hadal ocean sediments remain largely unexplored. In this study, we conducted single-cell genome sequencing on sediment samples collected from six sites (7,445-8,023 m water depth) along an approximately 500 km transect of the Japan Trench during the International Ocean Discovery Program Expedition 386. A total of 1,886 single-cell amplified genomes (SAGs) were obtained, offering comprehensive genetic insights into sedimentary microbial communities in surface sediments (<1 m depth) above the sulfate-methane transition zone along the Japan Trench. Our genome data set included 269 SAGs from Atribacterota JS1, the predominant bacterial clade in these hadal environments. Phylogenetic analysis classified SAGs into nine distinct phylotypes, whereas metagenome-assembled genomes were categorized into only two phylotypes, advancing JS1 diversity coverage through a single cell-based approach. Comparative genomic analysis of JS1 lineages from different habitats revealed frequent detection of genes related to organic carbon utilization, such as extracellular enzymes like clostripain and α-amylase, and ABC transporters of oligopeptide from Japan Trench members. Furthermore, specific JS1 phylotypes exhibited a strong correlation with in situ methane concentrations and contained genes involved in glycine betaine metabolism. These findings suggest that the phylogenomically diverse and novel Atribacterota JS1 is widely distributed in Japan Trench sediment, playing crucial roles in carbon cycling within the hadal sedimentary biosphere.IMPORTANCEThe Japan Trench represents tectonically active hadal environments associated with Pacific plate subduction beneath the northeastern Japan arc. This study, for the first time, documented a large-scale single-cell and metagenomic survey along an approximately 500 km transect of the Japan Trench, obtaining high-quality genomic information on hadal sedimentary microbial communities. Single-cell genomics revealed the predominance of diverse JS1 lineages not recoverable through conventional metagenomic binning. Their metabolic potential includes genes related to the degradation of organic matter, which contributes to methanogenesis in the deeper layers. Our findings enhance understanding of sedimentary microbial communities at water depths exceeding 7,000 m and provide new insights into the ecological role of biogeochemical carbon cycling in the hadal sedimentary biosphere.

Earthquake-enhanced dissolved carbon cycles in ultra-deep ocean sediments.

Hadal trenches are unique geological and ecological systems located along subduction zones. Earthquake-triggered turbidites act as efficient transport pathways of organic carbon (OC), yet remineralization and transformation of OC in these systems are not comprehensively understood. Here we measure concentrations and stable- and radiocarbon isotope signatures of dissolved organic and inorganic carbon (DOC, DIC) in the subsurface sediment interstitial water along the Japan Trench axis collected during the IODP Expedition 386. We find accumulation and aging of DOC and DIC in the subsurface sediments, which we interpret as enhanced production of labile dissolved carbon owing to earthquake-triggered turbidites, which supports intensive microbial methanogenesis in the trench sediments. The residual dissolved carbon accumulates in deep subsurface sediments and may continue to fuel the deep biosphere. Tectonic events can therefore enhance carbon accumulation and stimulate carbon transformation in plate convergent trench systems, which may accelerate carbon export into the subduction zones.

Subseafloor sulphide deposit formed by pumice replacement mineralisation.

Seafloor massive sulphide (SMS) deposits, modern analogues of volcanogenic massive sulphide (VMS) deposits on land, represent future resources of base and precious metals. Studies of VMS deposits have proposed two emplacement mechanisms for SMS deposits: exhalative deposition on the seafloor and mineral and void space replacement beneath the seafloor. The details of the latter mechanism are poorly characterised in detail, despite its potentially significant role in global metal cycling throughout Earth's history, because in-situ studies require costly drilling campaigns to sample SMS deposits. Here, we interpret petrographic, geochemical and geophysical data from drill holes in a modern SMS deposit and demonstrate that it formed via subseafloor replacement of pumice. Samples from the sulphide body and overlying sediment at the Hakurei Site, Izena Hole, middle Okinawa Trough indicate that sulphides initially formed as aggregates of framboidal pyrite and matured into colloform and euhedral pyrite, which were replaced by chalcopyrite, sphalerite and galena. The initial framboidal pyrite is closely associated with altered material derived from pumice, and alternating layers of pumiceous and hemipelagic sediments functioned as a factory of sulphide mineralisation. We infer that anhydrite-rich layers within the hemipelagic sediment forced hydrothermal fluids to flow laterally, controlling precipitation of a sulphide body extending hundreds of meters.

Temperature limits to deep subseafloor life in the Nankai Trough subduction zone.

Microorganisms in marine subsurface sediments substantially contribute to global biomass. Sediments warmer than 40°C account for roughly half the marine sediment volume, but the processes mediated by microbial populations in these hard-to-access environments are poorly understood. We investigated microbial life in up to 1.2-kilometer-deep and up to 120°C hot sediments in the Nankai Trough subduction zone. Above 45°C, concentrations of vegetative cells drop two orders of magnitude and endospores become more than 6000 times more abundant than vegetative cells. Methane is biologically produced and oxidized until sediments reach 80° to 85°C. In 100° to 120°C sediments, isotopic evidence and increased cell concentrations demonstrate the activity of acetate-degrading hyperthermophiles. Above 45°C, populated zones alternate with zones up to 192 meters thick where microbes were undetectable.