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Abiotic synthesis of methanethiol through CO2 reduction is a presumptive initiation reaction of protometabolism in primordial ocean hydrothermal systems. However, reported artificial means of methanethiol production indicate the necessity of gas-phase condition, rather than aqueous-phase setting, for this prebiotic reaction to occur. Here we show t...
A novel mesophilic bacterium, strain SS33 T , was isolated from a deep-sea hydrothermal vent chimney at Suiyo Seamount, Izu-Bonin Arc, Western Pacific Ocean. The cells of strain SS33 T were motile short rods with a single polar flagellum. The growth of strain SS33 T was observed at the temperature range between 33 and 55 °C (optimum growth at 45 °C...
Members of the kingdom Nanobdellati, previously known as DPANN archaea, are characterized by ultrasmall cell sizes and reduced genomes. They primarily thrive through ectosymbiotic interactions with specific hosts in diverse environments. Recent successful cultivations have emphasized the importance of adhesion to host cells for understanding the ec...
An anaerobic, mesophilic, syntrophic, archaeon strain MK-D1 T , was isolated as a pure co-culture with Methanogenium sp. strain MK-MG from deep-sea methane seep sediment. This organism is, to our knowledge, the first cultured representative of ‘Asgard’ archaea, an archaeal group closely related to eukaryotes. Here, we describe the detailed physiolo...
Archaeal cells are typically enveloped by glycosylated S-layer proteins. Archaeal protein glycosylation provides valuable insights not only into their adaptation to their niches but also into their evolutionary trajectory. Notably, thermophilic Thermoproteota modify proteins with N-glycans that include two GlcNAc units at the reducing end, resembli...
Deep-sea chemosynthetic ecosystems are ‘oases’ of life powered by reducing geofluids, of which serpentinite-hosted seeps are among the least studied. South Chamorro Seamount, a serpentine mud volcano on the Mariana Arc, has been known to host chemosynthesis-based assemblages since 1996, but no detailed information on the fauna was published. Here,...
A novel aerobic methanotrophic bacterium, designated as strain IN45 T , was isolated from in situ colonisation systems deployed at the Iheya North deep-sea hydrothermal field in the mid-Okinawa Trough. IN45 T was a moderately thermophilic obligate methanotroph that grew only on methane or methanol at temperatures between 25 and 56 °C (optimum 45–50...
A novel mesophilic bacterial strain, designated S502T, was isolated from a deep-sea hydrothermal vent at Suiyo Seamount, Japan. Cells were Gram-positive, asporogenous, motile, and curved rods, measuring 1.6–5.6 µm in length. The strain was an obligate anaerobe that grew fermentatively on complex substrates such as yeast extract and Bacto peptone. E...
Strictly hydrogen- and sulfur-oxidizing chemolithoautotrophic bacteria, particularly members of the phyla Campylobacterota and Aquificota, have a cosmopolitan distribution in deep-sea hydrothermal fields. The successful cultivation of these microorganisms in liquid media has provided insights into their physiological, evolutionary, and ecological c...
Infrared spectroscopy is used for the chemical characterization of prokaryotes. However, its application has been limited to cell aggregates and lipid extracts because of the relatively low spatial resolution of diffraction. We herein report optical photothermal infrared (O-PTIR) spectroscopy of prokaryotes for a domain-level diagnosis at the singl...
With the advance of high-throughput sequencing, the molecular basis of coevolutionary interaction between viruses and host microorganisms is predominantly elucidated by in silico genomic analyses, which revealed potential communication of genetic materials related to microbial immune systems such as the restriction-modification (R-M) system. Howeve...
A novel hyperthermophilic, heterotrophic archaeon, strain YC29T, was isolated from a deep-sea hydrothermal vent in the Mid-Okinawa Trough, Japan. Cells of strain YC29T were non-motile, irregular cocci with diameters of 1.2–3.0 µm. The strain was an obligatory fermentative anaerobe capable of growth on complex proteinaceous substrates. Growth was ob...
An increasing amount of evidence suggests that early ocean hydrothermal systems were sustained sources of ammonia, an essential nitrogen species for prebiotic synthesis of life’s building blocks. However, it remains a riddle how the abiotically generated ammonia was retained at the vent–ocean interface for the subsequent chemical evolution. Here, w...
A novel mesophilic, obligately anaerobic, facultatively sulphur-reducing bacterium, designated strain IC12T, was isolated from a deep-sea hydrothermal field in the Mid-Okinawa Trough, Japan. The cells were Gram-negative, motile, short rods with a single polar flagellum. The ranges and optima of the growth temperature, NaCl concentration and pH of s...
Lakes of molten sulfur are features sometimes found in seafloor hydrothermal vent systems. Daikoku of the northern Mariana Arc is notable for being home to one of such features inside its summit caldera, the “Sulfur Cauldron” discovered in 2006. A number of oceanographic research cruises since then have revealed significant volcanic activities on D...
Post-mega-earthquake geochemical and microbiological properties in subseafloor sediments of the Japan Trench accretionary wedge were investigated using core samples from Hole C0019E, which was drilled down to 851 m below seafloor (mbsf) at a water depth of 6,890 m. Methane was abundant throughout accretionary prism sediments; however, its concent...
Chemosynthetic ecosystems powered by microbial primary production are rare ‘hot spots’ of biological activity in the deep-sea characterized by dense aggregations of specially adapted animal species. Among settings where such systems have been found, serpentinite-hosted seep systems supported by alkaline geofluid are particularly understudied with j...
The Capitanian stage is characterized by marine anoxia possibly related to the extinction, although the global redox structure of the Capitanian ocean has not been constrained. We newly report a nitrogen isotope (δ¹⁵N) record from a paleo‐atoll limestone at the top of a mid‐Panthalassan seamount to constrain the spatial extent and duration of the C...
Polysulfide is a candidate for the redox pairs for thermocell devices; however, its aqueous solution has never been investigated. Polysulfides are in complex equilibria in an aqueous system, and the open-circuit potential of the solution is made of their mixed potential; thus, the dominant redox equilibrium determines its thermoelectric property. I...
A novel bacterium, strain MOT50T, was isolated from the chimney structure at the Iheya North field in the Mid-Okinawa Trough. The cells were motile short rods with a single polar flagellum. Growth was observed between 40 and 65 ℃ (optimum, 52 ℃), at pH values between 5.0 and 7.1 (optimum, pH 6.1) and in the presence of 2.0–4.0% NaCl (optimum, 2.5%)...
In deep-sea hydrothermal environments, inorganic sulfur compounds are important energy substrates for sulfur-oxidizing, -reducing, and -disproportionating microorganisms. Among these, sulfur-disproportionating bacteria have been poorly understood in terms of ecophysiology and phylogenetic diversity. Here, we isolated and characterized a novel mesop...
The genus Nitratiruptor represents one of the most numerically abundant chemolithoautotrophic Campylobacterota populations in the mixing zones of habitats between hydrothermal fluids and ambient seawater in deep-sea hydrothermal environments. We isolated and characterized four novel temperate phages (NrS-2, NrS-3, NrS-4, and NrS-5) having a siphovi...
Prebiotic chemical evolution and the emergence of life in the seafloor hydrothermal systems of Hadean Earth is among the most plausible and popular hypotheses for the origin of earthly life. In contrast, many studies pointed out that this hypothesis intrinsically harbors a critical unsolved problem called the “water paradox”: Abundant water limits...
Electroautotrophic microorganisms have attracted great attention since they exhibit a new type of primary production. Here, in situ electrochemical cultivation was conducted using the naturally occurring electromotive forces at a deep-sea hydrothermal vent. The voltage and current generation originating from the resulting microbial activity was obs...
In microbiology, cultivation is a central approach for uncovering novel physiology, ecology, and evolution of microorganisms, but conventional methods have left many microorganisms found in nature uncultured. To overcome the limitations of traditional methods and culture indigenous microorganisms, we applied a two-stage approach: enrichment/activat...
Carbonaceous matter (CM) in silica veins contained in the ~3.5 billion-year-old (Ga) Dresser Formation, Western Australia, can offer insights into biological activity in Earth’s oldest seafloor hydrothermal deposits, although a biological origin for this material remains debated. Herein, CM from Dresser hydrothermal vein deposits was analyzed using...
The hadal amphipod Hirondellea gigas is an emblematic animal of the Pacific trenches, and has a number of special adaptations to thrive in this ‘extreme’ environment, which includes the deepest part of the Earth’s ocean. One such adaptation that has been suggested is the presence of an ‘aluminum gel shield’ on the surface of its body in order to pr...
Raman and Fourier-transform infrared (FTIR) microspectroscopic analyses were performed to examine the chemical signatures and their spatial distribution of organic-walled microfossils together with organic matter (OM) in a black chert nodule from the Ediacaran (635–551 Ma) Doushantuo Formation in China. Raman spectral parameters (I-1350/1600 values...
Organisms use various forms and orientations of chitin nanofibres to make structures with a wide range of functions, from insect wings to mussel shells. Lophotrochozoan animals such as snails and annelid worms possess an ancient ‘biomineralization toolkit’, enabling them to flexibly and rapidly evolve unique hard parts. The scaly-foot snail is a ga...
The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields...
The Iheya North deep-sea hydrothermal field in the mid-Okinawa Trough is characterized by abundant methane derived from organic-rich sediments and diverse chemosynthetic animal species, including those harboring methanotrophic bacterial symbionts, such as bathymodiolin mussels Bathymodiolus japonicus and “ Bathymodiolus ” platifrons and a galatheoi...
H2‐rich ultramafic‐hosted hydrothermal systems are considered to be important places for the origin and early evolution of life. In this study, we conducted two hydrothermal serpentinization/carbonation experiments involving synthetic komatiite under CO2‐rich conditions to further understand the chemical nature of hydrothermal fluids in the komatii...
A novel mesophilic, strictly anaerobic, chemolithoautotrophic sulphate-reducing bacterium, designated strain KT2 T , was isolated from a deep-sea hydrothermal vent chimney at the Suiyo Seamount in the Izu-Bonin Arc. Strain KT2 T grew at 25–40 °C (optimum 35 °C) and pH 5.5–7.0 (optimum 6.6) in the presence of 25–45 g l ⁻¹ NaCl (optimum 30 g l ⁻¹ )....
Geological processes at subduction zones control seismicity, plutonism and volcanism, and geochemical cycling between the oceans, crust, and mantle. The down-going plate experiences metamorphism, and the associated dehydration and fluid flow alters the physical properties of the plate interface and mantle wedge, as well as controlling the compositi...
Abiotic fixation of atmospheric dinitrogen to ammonia is important in prebiotic chemistry and biological evolution in the Hadean and Archean oceans. Though it is widely accepted that nitrate (NO3−) was generated in the early atmospheres, the stable pathways of ammonia production from nitrate deposited in the early oceans remain unknown. This paper...
A prevailing scenario of the origin of life postulates thioesters as key intermediates in protometabolism, but there is no experimental support for the prebiotic CO2 fixation routes to thioesters. Here we demonstrate that, under a simulated geoelectrochemical condition in primordial ocean hydrothermal systems (–0.6 to –1.0 V versus the standard hyd...
A novel thermophilic bacterium, strain SSM-sur55T, was isolated from a chimney structure at the Urashima site on the Southern Mariana Trough in the Pacific Ocean. Growth was observed at temperatures between 25 and 60 °C (optimum, 55 °C; 180 min doubling time), at pH values between 5.3 and 7.2 (optimum, pH 5.9) and in the presence of between 1.6 and...
Seafloor cratering is an important process that records the impact history of the Earth, affects projectile survivability, and determines the mass of ejecta from benthic rock that is transported to the atmosphere. We report experimental hypervelocity impacts of chondrite and other projectiles (olivine, stainless‐steel, polycarbonate) on a water‐cov...
A mannan-degrading halophilic archaeal strain, MD130-1 T , was isolated from a commercial salt sample. Cells were motile, rod-shaped, and stained Gram-negative. Colonies were pink pigmented. Strain MD130-1 T was able to grow at 1.5–4.6 M NaCl (optimum, 3.6 M) at pH 6.0–8.0 (optimum, pH 7.0) and at 25–50 °C (optimum, 40 °C). The DNA G+C content was...
Deep-sea hydrothermal vent ecosystems remain mysterious. To depict in detail the enigmatic life of chemosynthetic microbes, which are key primary producers in these ecosystems, metatranscriptomic analysis is expected to be a promising approach. However, this has been hindered by substantial perturbation (e.g., RNA degradation) during time-consuming...
Thioester synthesis by CO dehydrogenase/acetyl-CoA synthase is among the most ancient autotrophic metabolisms. Although the preceding prebiotic CO2 fixation routes to thioesters are often suggested, none has any experimentally supported evidence. Here we demonstrate that, under an electrochemical condition realizable in early ocean hydrothermal sys...
Nitrous oxide (N2O) is a potent greenhouse gas and has significantly increased in the atmosphere. Deep-sea hydrothermal fields are representative environments dominated by mesophilic to thermophilic members of the class Campylobacteria that possess clade II nosZ encoding nitrous oxide reductase. Here, we report a strain HRV44T representing the firs...
NDP-forming type acyl-CoA synthetase superfamily proteins are known to have six essential subdomains (1, 2, 3, a, b, c) of which partition and order are varied, suggesting yet-to-be-defined subdomain rearrangement happened in its evolution. Comparison in physicochemical and biochemical characteristics between the recombinant proteins which we made...
The Scaly-foot Snail, Chrysomallon squamiferum, presents a combination of biomineralised features, reminiscent of enigmatic early fossil taxa with complex shells and sclerites such as sachtids, but in a recently-diverged living species which even has iron-infused hard parts. Thus the Scaly-foot Snail is an ideal model to study the genomic mechanism...
Some deep-sea chemosynthetic invertebrates and their symbiotic bacteria can use molecular hydrogen (H2) as their energy source. However, how much the chemosynthetic holobiont (endosymbiont-host association) physiologically depends on H2 oxidation has not yet been determined. Here, we demonstrate that the Campylobacterota endosymbionts of the gastro...
The origin of eukaryotes remains unclear1–4. Current data suggest that eukaryotes may have emerged from an archaeal lineage known as ‘Asgard’ archaea5,6. Despite the eukaryote-like genomic features that are found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear, owing to the lack of cultured representatives a...
The subduction of seamounts and ridge features at convergent plate boundaries plays an important role in the deformation of the overriding plate and influences geochemical cycling and associated biological processes. Active serpentinization of forearc mantle and serpentinite mud volcanism on the Mariana forearc (between the trench and active volcan...
Hadal trench bottom (>6000 m below sea level) sediments harbor higher microbial cell abundance compared with adjacent abyssal plain sediments. This is supported by the accumulation of sedimentary organic matter (OM), facilitated by trench topography. However, the distribution of benthic microbes in different trench systems has not been well explore...
Chemical evolution is an abiotic reaction process in which complex organic molecules arise from a combination of simple inorganic and organic chemical compounds. To assess the possible ongoing chemical evolution in the subsurface ocean of Saturn’s icy satellite Enceladus, we explored the water-rock aqueous reactions and the peptide formation capabi...
Significance
Highly adapted to deep-sea hot vents, the scaly-foot gastropod Chrysomallon squamiferum is unique among living and extinct animals in possessing an imbricating scale-armor reinforced by iron sulfide nanoparticles. Mechanisms behind its biogenic sulfide synthesis are expected to revolutionize industrial production of metal chalcogenide...
Hadal trench bottom (>6,000 m below sea level) sediments harbor higher microbial cell abundance compared to adjacent abyssal plain sediments. This is supported by the accumulation of sedimentary organic matter (OM), facilitated by trench topography. However, the distribution of benthic microbes in different trench systems has not been explored yet....
The origin of eukaryotes remains enigmatic. Current data suggests that eukaryotes may have risen from an archaeal lineage known as "Asgard archaea". Despite the eukaryote-like genomic features found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear due to the lack of cultured representatives and corresponding...
Serpentinitic systems are potential habitats for microbial life due to frequently high concentrations of microbial energy substrates, such as hydrogen (H2), methane (CH4), and short-chain organic acids (SCOAs). Yet, many serpentinitic systems are also physiologically challenging environments due to highly alkaline conditions (pH > 10) and elevated...
Conventional and synchrotron radiation‐based (SR) Fourier transform infrared microspectroscopies (micro‐FTIR) were applied to four types of ~ 810 Ma organic‐walled microfossils together with diffuse organic matter (OM) and one irregularly shaped structure from the Fifteenmile Group, in Yukon, Canada, for their chemical characterization. The microfo...
Viruses are the most abundant biological entities on Earth and perform essential ecological functions in aquatic environments by mediating biogeochemical cycling and lateral gene transfer. Cellular life as well as viruses have been found in deep subseafloor sediment. However, the study of deep sediment viruses has been hampered by the complexities...
A novel hydrogenotrophic methanogen, strain HHBT, was isolated from a deep-sea hydrothermal vent chimney sample collected from Beebe Vent Field at the Mid-Cayman Spreading Center, Caribbean Sea. The cells were non-motile regular to irregular cocci possessing several flagella. The novel isolate grew at 60-80 °C, pH 5.0-7.4 and with 1-4 % of NaCl (w/...
Recent explorations of scientific ocean drilling have revealed the presence of microbial communities persisting in sediments down to ~2.5 km below the ocean floor. However, our knowledge of these microbial populations in the deep subseafloor sedimentary biosphere remains limited. Here, we present a cultivation experiment of 2-km-deep subseafloor mi...
A novel slow-growing, facultatively anaerobic, filamentous bacterium, strain MO-CFX2T, was isolated from a methanogenic microbial community in a continuous-flow bioreactor that was established from subseafloor sediment collected off the Shimokita Peninsula of Japan. Cells were multicellular filamentous, non-motile and Gram-stain-negative. The filam...
Serpentinite-hosting mud volcanoes, located in the Marianna forearc subduction zone, were drilled during IODP Expedition 366. Recovered samples from Asùt Tesoru seamount provide new insights on the generation of organic matter in deep environments. Short-chain alcohols, volatile fatty acids and light hydrocarbons are produced within hyperalkaline p...
Studying the diversity of extant metabolisms and enzymes, especially those involved in the biosynthesis of primary metabolites including amino acids, is important to shed light on the evolution of life. Many organisms synthesize serine from phosphoserine via a reaction catalyzed by phosphoserine phosphatase (PSP). Two types of PSP, belonging to dis...
