Deep-sea Hydrothermal Environments Research Articles

Speciation of iodine on biogenic iron oxyhydroxides by I K-edge and LIII-edge XANES

Abstract The host phase of iodine (I) in biogenic iron oxyhydroxides (BIOS) was determined using X-ray absorption near-edge structure (XANES). I K-edge and LIII-edge XANES analyses of BIOS collected from deep-sea hydrothermal environments revealed that the primary form of I in the BIOS is an organic species. Furthermore, LIII-edge XANES fitting implied the dominance of aromatic-bound I among BIOS. Our first observation of organic–trace element association in natural BIOS can explain the enhanced adsorption of I on BIOS compared to synthetic ferrihydrite. This further suggests the importance of various chemistry on this organic–mineral composite for understanding the geochemical cycling of trace elements.

Insights into the bacterial and archaeal population dynamics in the deep-sea hydrothermal sediments exposed to lights with different wavelengths

The deep-sea hydrothermal environments with steep temperature and chemical gradients foster a rich microbial diversity. The presence of infrared light and bioluminescence in the hydrothermal fields has been reported. However, effects of illumination on the growth of the microorganisms in the deep-sea hydrothermal environments have not been studied. In this work, metagenomic analysis of hydrothermal sediment samples was performed and the data showed that genes of photosensitive proteins are widely distributed, indicating that light might be a crucial environmental factor for cultivation of hydrothermal microorganisms. To further study the effects of light on enrichment and culture of hydrothermal microorganisms, sediment samples collected from deep-sea hydrothermal fields were cultured under the conditions of dark, white light, blue light, green light, red light and infrared light, respectively. Then, the V4-V5 regions of 16S rRNA genes of bacteria and archaea were sequenced through high-throughput sequencing, and the microbial community composition of bacteria and archaea in different samples was studied. The results showed that different species of microorganisms were enriched under different light conditions. Notably, there were significant differences in microbial composition under dark and other light conditions, suggesting that light is an important signal for growth and culture of hydrothermal microorganisms. Overall, this study shed light on the function of lights on the culture of hydrothermal microorganisms.

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

BackgroundWhen deep-sea hydrothermal fluids mix with cold oxygenated fluids, minerals precipitate out of solution and form hydrothermal deposits. These actively venting deep-sea hydrothermal deposits support a rich diversity of thermophilic microorganisms which are involved in a range of carbon, sulfur, nitrogen, and hydrogen metabolisms. Global patterns of thermophilic microbial diversity in deep-sea hydrothermal ecosystems have illustrated the strong connectivity between geological processes and microbial colonization, but little is known about the genomic diversity and physiological potential of these novel taxa. Here we explore this genomic diversity in 42 metagenomes from four deep-sea hydrothermal vent fields and a deep-sea volcano collected from 2004 to 2018 and document their potential implications in biogeochemical cycles.ResultsOur dataset represents 3635 metagenome-assembled genomes encompassing 511 novel and recently identified genera from deep-sea hydrothermal settings. Some of the novel bacterial (107) and archaeal genera (30) that were recently reported from the deep-sea Brothers volcano were also detected at the deep-sea hydrothermal vent fields, while 99 bacterial and 54 archaeal genera were endemic to the deep-sea Brothers volcano deposits. We report some of the first examples of medium- (≥ 50% complete, ≤ 10% contaminated) to high-quality (> 90% complete, < 5% contaminated) MAGs from phyla and families never previously identified, or poorly sampled, from deep-sea hydrothermal environments. We greatly expand the novel diversity of Thermoproteia, Patescibacteria (Candidate Phyla Radiation, CPR), and Chloroflexota found at deep-sea hydrothermal vents and identify a small sampling of two potentially novel phyla, designated JALSQH01 and JALWCF01. Metabolic pathway analysis of metagenomes provides insights into the prevalent carbon, nitrogen, sulfur, and hydrogen metabolic processes across all sites and illustrates sulfur and nitrogen metabolic “handoffs” in community interactions. We confirm that Campylobacteria and Gammaproteobacteria occupy similar ecological guilds but their prevalence in a particular site is driven by shifts in the geochemical environment.ConclusionOur study of globally distributed hydrothermal vent deposits provides a significant expansion of microbial genomic diversity associated with hydrothermal vent deposits and highlights the metabolic adaptation of taxonomic guilds. Collectively, our results illustrate the importance of comparative biodiversity studies in establishing patterns of shared phylogenetic diversity and physiological ecology, while providing many targets for enrichment and cultivation of novel and endemic taxa.6aUVBDbDZ6m8Eohc79dCDgVideo

Physiological and comparative proteomic characterization of Desulfolithobacter dissulfuricans gen. nov., sp. nov., a novel mesophilic, sulfur-disproportionating chemolithoautotroph from a deep-sea hydrothermal vent.

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 mesophilic, strictly chemolithoautotrophic, diazotrophic sulfur-disproportionating bacterium, designated strain GF1T, from a deep-sea hydrothermal vent chimney at the Suiyo Seamount in the Izu-Bonin Arc, Japan. Strain GF1T disproportionated elemental sulfur, thiosulfate, and tetrathionate in the presence of ferrihydrite. The isolate also grew by respiratory hydrogen oxidation coupled to sulfate reduction. Phylogenetic and physiological analyses support that strain GF1T represents the type strain of a new genus and species in the family Desulfobulbaceae, for which the name Desulfolithobacter dissulfuricans gen. nov. sp. nov. is proposed. Proteomic analysis revealed that proteins related to tetrathionate reductase were specifically and abundantly produced when grown via thiosulfate disproportionation. In addition, several proteins possibly involved in thiosulfate disproportionation, including those encoded by the YTD gene cluster, were also found. The overall findings pointed to a possible diversity of sulfur-disproportionating bacteria in hydrothermal systems and provided a refined picture of microbial sulfur disproportionation.

Genomic insights into phage-host interaction in the deep-sea chemolithoautotrophic Campylobacterota, Nitratiruptor

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 siphoviral morphology, infecting Nitratiruptor strains from the Hatoma Knoll hydrothermal field in the southern-Okinawa Trough, Japan, and conducted comparative genomic analyses among Nitratiruptor strains and their phages. The Nitratiruptor temperate phages shared many potential core genes (e.g., integrase, Cro, two structural proteins, lysozyme, and MazG) with each other despite their diverse morphological and genetic features. Some homologs of coding sequences (CDSs) of the temperate phages were dispersed throughout the non-prophage regions of the Nitratiruptor genomes. In addition, several regions of the phage genome sequences matched to spacer sequences within clustered regularly interspaced short palindromic repeats (CRISPR) in Nitratiruptor genomes. Moreover, a restriction-modification system found in a temperate phage affected an epigenetic feature of its host. These results strongly suggested a coevolution of temperate phages and their host genomes via the acquisition of temperate phages, the CRISPR systems, the nucleotide substitution, and the epigenetic regulation during multiple phage infections in the deep-sea environments.

In situ electrosynthetic bacterial growth using electricity generated by a deep-sea hydrothermal vent

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 observed for 12 days of deployment, with fluctuation in response to tidal cycles. A novel bacterium belonging to the genus Thiomicrorhabdus dominated the microbial community specifically enriched on the cathode. Metagenomic analysis provided the draft genome of the bacterium and the gene repertoire indicated that the bacterium has the potential for thio-autotrophic growth, which is a typical physiological feature of the members of the genus, while the bacterium had a unique gene cluster encoding multi-heme cytochrome c proteins responsible for extracellular electron transfer. Herein, we propose this bacterium as a new species, specifically enriched during electricity generation, as ‘Candidatus Thiomicrorhabdus electrophagus’. This finding suggests the natural occurrence of electrosynthetic microbial populations using the geoelectricity in deep-sea hydrothermal environments.

Genomic patterns of divergence in the early and late steps of speciation of the deep-sea vent thermophilic worms of the genus Alvinella

BackgroundThe transient and fragmented nature of the deep-sea hydrothermal environment made of ridge subduction, plate collision and the emergence of new rifts is currently acting to separate of vent populations, promoting local adaptation and contributing to bursts of speciation and species specialization. The tube-dwelling worms Alvinella pompejana called the Pompeii worm and its sister species A. caudata live syntopically on the hottest part of deep-sea hydrothermal chimneys along the East Pacific Rise. They are exposed to extreme thermal and chemical gradients, which vary greatly in space and time, and thus represent ideal candidates for understanding the evolutionary mechanisms at play in the vent fauna evolution.ResultsWe explored genomic patterns of divergence in the early and late stages of speciation of these emblematic worms using transcriptome assemblies and the first draft genome to better understand the relative role of geographic isolation and habitat preference in their genome evolution. Analyses were conducted on allopatric populations of Alvinella pompejana (early stage of separation) and between A. pompejana and its syntopic species Alvinella caudata (late stage of speciation). We first identified divergent genomic regions and targets of selection as well as their position in the genome over collections of orthologous genes and, then, described the speciation dynamics by documenting the annotation of the most divergent and/or positively selected genes involved in the isolation process. Gene mapping clearly indicated that divergent genes associated with the early stage of speciation, although accounting for nearly 30% of genes, are highly scattered in the genome without any island of divergence and not involved in gamete recognition or mito-nuclear incompatibilities. By contrast, genomes of A. pompejana and A. caudata are clearly separated with nearly all genes (96%) exhibiting high divergence. This congealing effect however seems to be linked to habitat specialization and still allows positive selection on genes involved in gamete recognition, as a possible long-duration process of species reinforcement.ConclusionOur analyses highlight the non-negligible role of natural selection on both the early and late stages of speciation in the iconic thermophilic worms living on the walls of deep-sea hydrothermal chimneys. They shed light on the evolution of gene divergence during the process of speciation and species specialization over a very long period of time.

Complete genome sequence of Roseivivax marinus strain TCYB24 with quorum sensing system reveal the adaptive mechanism against deep-sea hydrothermal environment.

Roseivivax marinus strain TCYB24 is a rod-shaped bacterium of Rhodobacteraceae isolated from the gill of deep-sea mussel Bathymodiolus marisindicus which collected from the Tiancheng hydrothermal vent under depth of 2700m on the southwest Indian ridge. In our previous study, the strain TCYB24 was proved to produce quorum sensing signal of N-Acyl-homoserine lactones (AHLs) and form biofilm. In order to determine its adaptive mechanism against the extreme environment of deep-sea hydrothermal vents, the whole genome was sequenced by high-throughput Illumina tag sequencing. The results show the whole genome consists of one circular chromosome and eight circular plasmids, with a total length of 4.60Mb (G+C content of 67.4%), 4338 open reading frames, 46 tRNAs and 6 rRNA operons. According to the genome-wide functional annotation, numbers of heavy metal resistance, high pressure and cold adapting related genes were found. In addition, genes about exopolysaccharide (EPS) biosynthesis and secretion and biofilm formation, which facilitate bacteria to resist extreme environments, were identified. Intriguingly, a pair of RaiI/R-type quorum sensing system was discovered firstly in the bacterium isolated from hydrothermal environment. The results may help to understand genetic underpinning of extreme environmental adaptation mechanism of bacteria in deep-sea hydrothermal area.

Research Progress on Corrosion of Equipment and Materials in Deep-Sea Environment

The deep sea is the frontier of materials research in the 21st century. Owing to the particularity of pressure (15–120 MPa), hydrothermal temperature (90–400°C), and explosive fluid (strong H2S) in the deep-sea hydrothermal field environment, the research on the corrosion mechanism of service materials in this environment under the coupling action of many harsh factors is almost blank. It has become the bottleneck of equipment and material research and development for China to explore the deep sea. This paper reviews the research progress of corrosion mechanisms of deep-sea environmental materials at home and abroad, and forecasts the research trend and difficulties in this field, especially in the deep-sea hydrothermal field. At the same time, it points out the urgency of the construction of harsh environment materials platform and its relevance to the discipline construction of marine college.

Biochemical and metabolic responses of the deep-sea mussel Bathymodiolus platifrons to cadmium and copper exposure

Greater interest in commercial deep-sea mining has been accompanied by mounting environmental concerns, including metal contamination resulting from mining activities. However, little is known about the toxic effects of metal exposure on deep-sea life. Given its ability to accumulate metals from the surrounding environment, its wide distribution at both vents and seeps, and its high abundance, the deep-sea mussel Bathymodiolus platifrons could serve as an ideal model to investigate the toxicological responses of deep-sea organisms to metal exposure. Here, we evaluated metal accumulation, traditional metal-related biomarkers, namely acid phosphatase (ACP), alkaline phosphatase (AKP), superoxide dismutase, catalase, reduced glutathione, metallothioneins, and malondialdehyde, as well as metabolic profiles in the gills of B. platifrons after a 7-day exposure to copper (100 μg/L), cadmium (500 μg/L), or copper-plus-cadmium treatments (100 μg/L Cu and 500 μg/L Cd). Metal exposure concentrations selected in this study can be found in deep-sea hydrothermal environments. Metal exposure resulted in significant metal accumulation in the gills of the mussel, indicating that B. platifrons has promise for use as an indicator of deep-sea metal pollution levels. Traditional biomarkers (AKP, ACP, and measured antioxidants) revealed cellular injury and oxidative stress in mussels following metal exposure. Metabolic responses in the three treatment groups indicated that metal exposure perturbed osmoregulation, energy metabolism, and nucleotide metabolism in mussels, in a response marked by differentially altered levels of amino acids, hypotaurine, betaine, succinate, glucose 6-phosphate, fructose 6-phosphate, guanosine, guanosine 5′-monophosphate, and inosine. Nevertheless, several uniquely altered metabolites were found in each treatment exposure group, suggesting dissimilar modes of toxicity between the two metal types. In the Cd-exposed group, the monosaccharide D-allose, which is involved in suppressing mitochondrial ROS production, was downregulated, a response consistent with oxidative stress in Cd-exposed B. platifrons. In the Cu-exposed group, the detected alterations in dopamine, dopamine-related, and serotonin-related metabolites together suggest disturbed neurotransmission in Cu-exposed B. platifrons. In the Cu-plus-Cd group, we detected a decline in fatty acid levels, implying that exposure to both metals jointly exerted a negative influence on the physiological functioning of the mussel. To the best of our knowledge, this is the first study to investigate changes in metabolite profiles in Bathymodiolus mussels exposed to metal. The findings reported here advance our understanding of the adverse impact of metal exposure on deep-sea life and can inform deep-sea mining assessments through the use of multiple biomarkers.

Optimal Design for Higher Resistance to Thermal Impulse: A Lesson Learned from the Shells of Deep-Sea Hydrothermal-Vent Snails

Inspired by the unique design of the shells of snails inhabiting the deep-sea hydrothermal environment, here we theoretically study the temperature response of a bilayer to an external thermal impulse. A semi-analytical solution to the temperature field in the bilayer is obtained, allowing us to assess the peak temperature that occurs on the inner wall as a quantitative indicator of the thermal resistance of the bilayer. The structural determining factors of the thermal resistance of a bilayer are then investigated by examining the effects of the stacking sequence and volume fractions of the constitutive layers on the peak temperature on the inner wall. Our results indicate that the stacking sequence of the two layers in a bilayer, as well as their volume fractions, play important roles in determining the thermal resistance. For two layers with given materials, there exists an optimal stacking sequence and thickness ratio giving rise to the best thermal resistance. The results of our work not only account for the unique laminated design of the snail shells from hydrothermal environments but also provide practical guidelines for the design of multilayer thermal barriers in engineering.

Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas.

Bacteria of the genus Sulfurimonas within the class Campylobacteria are predominant in global deep-sea hydrothermal environments and widespread in global oceans. However, only few bacteria of this group have been isolated, and their adaptations for these extreme environments remain poorly understood. Here, we report a novel mesophilic, hydrogen- and sulfur-oxidizing bacterium, strain NW10T, isolated from a deep-sea sulfide chimney of Northwest Indian Ocean.16S rRNA gene sequence analysis showed that strain NW10T was most closely related to the vent species Sulfurimonas paralvinellae GO25T with 95.8% similarity, but ANI and DDH values between two strains were only 19.20 and 24.70%, respectively, indicating that strain NW10 represents a novel species. Phenotypic characterization showed strain NW10T is an obligate chemolithoautotroph utilizing thiosulfate, sulfide, elemental sulfur, or molecular hydrogen as energy sources, and molecular oxygen, nitrate, or elemental sulfur as electron acceptors. Moreover, hydrogen supported a better growth than reduced sulfur compounds. During thiosulfate oxidation, the strain can produce extracellular sulfur of elemental α-S8 with an unknown mechanism. Polyphasic taxonomy results support that strain NW10T represents a novel species of the genus Sulfurimonas, and named as Sulfurimonas hydrogeniphila sp. nov. Genome analyses revealed its diverse energy metabolisms driving carbon fixation via rTCA cycling, including pathways of sulfur/hydrogen oxidation, coupled oxygen/sulfur respiration and denitrification. Comparative analysis of the 11 available genomes from Sulfurimonas species revealed that vent bacteria, compared to marine non-vent strains, possess unique genes encoding Type V Sqr, Group II, and Coo hydrogenase, and are selectively enriched in genes related to signal transduction and inorganic ion transporters. These phenotypic and genotypic features of vent Sulfurimonas may explain their thriving in hydrothermal environments and help to understand the ecological role of Sulfurimonas bacteria in hydrothermal ecosystems.

Complete genome sequence and comparative genome analysis of Alcanivorax sp. IO_7, a marine alkane-degrading bacterium isolated from hydrothermally-influenced deep seawater of southwest Indian ridge

Genome of Alcanivorax sp. IO_7, an alkane degrading deep-sea bacteria isolated from hydrothermally-influenced Southwest Indian Ridge was sequenced and analysed. Genomic data mining revealed gene clusters for degrading n-alkane and cycloalkanes, including biosurfactant production. The strain was shown to grow on hexadecane as its sole carbon source, supporting the findings of genomic analysis. Presence of cyclohexanone monooxygenase among genomic islands suggest that this strain may have used gene transfer to enhance its hydrocarbon degradation ability. Genes encoding for heavy metal resistance, multidrug resistance and multiple natural product biosynthesis crucial for survival in the hydrothermally influenced deep sea environment were detected. In our comparative genome analysis, it was evident that marine Alcanivorax strains contain a suite of enzymes for n-alkane and haloalkanoate degradation. Comparative genome and genomic synteny analysis provided insights into the physiological features and adaptation strategies of Alcanivorax sp. IO_7 in the deep-sea hydrothermal environment.

Elemental sulfur reduction by a deep-sea hydrothermal vent Campylobacterium Sulfurimonas sp. NW10.

Sulfurimonas species (class Campylobacteria, phylum Campylobacterota) were globally distributed and especially predominant in deep-sea hydrothermal environments. They were previously identified as chemolithoautotrophic sulfur-oxidizing bacteria (SOB), whereas little is known about their potential in sulfur reduction. In this report, we found that the elemental sulfur reduction is quite common in different species of genus Sulfurimonas. To gain insights into the sulfur reduction mechanism, growth tests, morphology observation, as well as genomic and transcriptomic analyses were performed on a deep-sea hydrothermal vent bacterium Sulfurimonas sp. NW10. Scanning electron micrographs and dialysis tubing tests confirmed that elemental sulfur reduction occurred without direct contact of cells with sulfur particles while direct access strongly promoted bacterial growth. Furthermore, we demonstrated that most species of Sulfurimonas probably employ both periplasmic and cytoplasmic polysulfide reductases, encoded by genes psrA1 B1 CDE and psrA2 B2 , respectively, to accomplish cyclooctasulfur reduction. This is the first report showing two different sulfur reduction pathways coupled to different energy conservations could coexist in one sulfur-reducing microorganism, and demonstrates that most bacteria of Sulfurimonas could employ both periplasmic and cytoplasmic polysulfide reductases to perform cyclooctasulfur reduction. The capability of sulfur reduction coupling with hydrogen oxidation may partially explain the prevalenceof Sulfurimonas in deep-sea hydrothermal vent environments.

Biogeochemical Implications of N2O-Reducing Thermophilic Campylobacteria in Deep-Sea Vent Fields, and the Description of Nitratiruptor labii sp. nov.

SummaryNitrous 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 first thermophilic campylobacterium capable of growth by H2 oxidation coupled to N2O reduction. On the basis of physiological and genomic properties, it is proposed that strain HRV44T (=JCM 34002 = DSM 111345) represents a novel species of the genus Nitratiruptor, Nitratiruptor labii sp. nov. The comparison of the N2O consumption ability of strain HRV44T with those of additional Nitratiruptor and other campylobacterial strains revealed the highest level in strain HRV44T and suggests the N2O-respiring metabolism might be the common physiological trait for the genus Nitratiruptor. Our findings provide insights into contributions of thermophilic Campylobacteria to the N2O sink in deep-sea hydrothermal environments.

Complete genome sequence of Methanofervidicoccus sp. A16, a thermophilic methanogen isolated from Mid Cayman Rise hydrothermal vent.

Methanofervidicoccus sp. A16 is a novel thermophilic and obligate hydrogenotrophic methanogen isolated from a deep-sea hydrothermal vent chimney sample at the Mid Cayman spreading center, Caribbean Sea. Here we report the complete genome of strain A16, which has one circular chromosome of 1,485,358bp with a mean G+C content of 35.01mol%. The complete genome harbors 1442 predicted protein-encoding genes. Genes involved in hydrogenotrophic methane production and N2 fixation were identified in this genome. This study expands our knowledge of methanogenesis at high temperatures and the involvement of these microorganisms in the carbon and nitrogen cycles of deep-sea hydrothermal environments.

Characterization of the Genome Feature and Toxic Capacity of a Bacillus wiedmannii Isolate From the Hydrothermal Field in Okinawa Trough

The Bacillus cereus group is frequently isolated from soil, plants, food, and other environments. In this study, we report the first isolation and characterization of a B. cereus group member, Bacillus wiedmannii SR52, from the hydrothermal field in the Iheya Ridge of Okinawa Trough. SR52 was isolated from the gills of shrimp Alvinocaris longirostris, an invertebrate species found abundantly in the ecosystems of the hydrothermal vents, and is most closely related to B. wiedmannii FSL W8-0169. SR52 is aerobic, motile, and able to form endospores. SR52 can grow in NaCl concentrations up to 9%. SR52 has a circular chromosome of 5,448,361 bp and a plasmid of 137,592 bp, encoding 5,709 and 189 genes, respectively. The chromosome contains 297 putative virulence genes, including those encoding enterotoxins and hemolysins. Fourteen rRNA operons, 107 tRNAs, and 5 sRNAs are present in the chromosome, and 7 tRNAs are present in the plasmid. SR52 possesses 13 genomic islands (GIs), all on the chromosome. Comparing to FSL W8-0169, SR52 exhibits several streaking features in its genome, notably an exceedingly large number of non-coding RNAs and GIs. In vivo studies showed that following intramuscular injection into fish, SR52 was able to disseminate in tissues and cause mortality; when inoculated into mice, SR52 induced acute mortality and disseminated transiently in tissues. In vitro studies showed that SR52 possessed hemolytic activity, and the extracellular product of SR52 exhibited a strong cytotoxic effect. These results provided the first insight into the cytotoxicity and genomic feature of B. wiedmannii from the deep-sea hydrothermal environment.

Diversity and metabolism of prokaryotic chemoautotrophs and their interactions with deep-sea hydrothermal environments

The deep sea hydrothermal vent ecosystem was first discovered in 1977 at East Pacific Rise (EPR) near the Galapagos Islands. In the past decades, over 640 hydrothermal vent sites have been found in oceans, a majority of which have been found on the mid-ocean ridges. Chinese scientists have contributed significantly to the discovery of new sites on the Southwest Indian Ridge and South Mid-Atlantic Ridge. Due to worldwide oceanic expeditions, significant advances have been made in the observation of hydrothermal vent ecosystems, regarding the diversity and geographical distribution of vent fauna and microbial communities. The vent chemolithoautotrophs and their symbiosis with vent clams, mussels, tube worms and shrimps, in particular, gained more attention. In this paper, recent advances in diversity and versatile metabolisms of prokaryotic chemoautotrophs are reviewed. The vent chemolithoautotrophs are pivotal in the cross-connected interactions of abiotic and biotic processes. They act as the primary producer in the unique ecosystem driven by the deep dark energy derived from water-rock reaction around the magma chamber. Correspondingly, various chemoautotrophic bacteria are capable of utilizing the reduced compounds generated by water-rock reaction, via sulfur oxidization, methane oxidization, hydrogen oxidization, iron oxidization and ammonia oxidization; in contrast, chemoautotrophic vent archaea tend to harness energy from hydrogen in the inner part of the hydrothermal chimney coupling with sulfur reduction. In addition, heterotrophic archaea of Thermococcales also frequently occurs in high temperature chimneys; while some archaea can oxidize ammonia and methane in the vent surroundings. These diverse prokaryotes selectively distribute in a variety of vent niches along the steep environmental gradients of temperature, pH, Eh and concentrations of the reduced compounds. In the case of a black smoke ecosystem, where the hydrogen sulfide in hydrothermal fluids is effluent, sulfur oxidation is recognized as a major process driving carbon fixation for primary production; while in the mixing zones, the partially oxidized inorganic sulfur compounds like thiosulfate and polysulfide can be further oxidized by sulfur-oxidizing bacteria (SOB). Among them, Epsilonproteobacteria such as Sulfurimonas, Sulfurovum, Arcobacter , Hydrogenovibrio and Thiomicrospira are predominant genera of SOBs in plume-mixed seawater close to the vent, while bacteria of Gammaproteobacteria SUP05 clade are relatively abundant in the cold oxidized seawater farther away from the vent. In the case of the white chimney, methane-metabolizing archaea of Methanosarcinales and hydrogen- oxidizing Thiomicrospira dominate the prokaryotic community in microbial mat. In addition, another group of chemolithoautotrophs function as endo- and epi-symbionts of vent animals that are essential to the health of vent ecosystem; these symbionts mostly belong to sulfur, hydrogen and methane oxidizers. However, all these processes need quantification to evaluate the efflux of energy and synthesized organic compounds. Considering the global distribution and the immense influence in respect to continuous efflux of energy and substances, hydrothermal vents play an important role in life evolution. Both geological records and computational analysis reveal that early life on Earth is likely originated from the deep hydrothermal system, with features of anaerobic, thermophilic, hydrogen-oxidizing, coupled with carbon and nitrogen fixation, represented by the Last Universal Common Ancestor (LUCA). Because of our limited knowledge about the deep biosphere along with deep time evolution, more efforts are needed to investigate the dark ecosystem with integrated approaches, to project the nature of life in dark with unique mechanisms, and to finally elucidate the origin and evolution of life on earth.

Enrichment and Genomic Characterization of a N2O-Reducing Chemolithoautotroph From a Deep-Sea Hydrothermal Vent.

Nitrous oxide (N2O) is a greenhouse gas and also leads to stratospheric ozone depletion. In natural environments, only a single N2O sink process is the microbial reduction of N2O to N2, which is mediated by nitrous oxide reductase (NosZ) encoded by nosZ gene. The nosZ phylogeny has two distinct clades, clade I and formerly overlooked clade II. In deep-sea hydrothermal environments, several members of the class Campylobacteria are shown to harbor clade II nosZ gene and perform the complete denitrification of nitrate to N2; however, little is known about their ability to grow on exogenous N2O as the sole electron acceptor. Here, we obtained an enrichment culture from a deep-sea hydrothermal vent in the Southern Mariana Trough, which showed a respiratory N2O reduction with H2 as an electron donor. The single amplicon sequence variant (ASV) presenting 90% similarity to Hydrogenimonas species within the class Campylobacteria was predominant throughout the cultivation period. Metagenomic analyses using a combination of short-read and long-read sequence data succeeded in reconstructing a complete genome of the dominant ASV, which encoded clade II nosZ gene. This study represents the first cultivation analysis that shows the occurrence of N2O-respiring microorganisms in a deep-sea hydrothermal vent and provides the opportunity to assess their capability to reduce N2O emission from the environments.

(Invited) De-Coupled Electron and Heat Transfer: A Possible Nature’s Strategy for Maximizing Electrocatalysis for CO2 Fixation

How has nature handled electron flow for carbon fixation? We know the mechanism of carbon fixation taking place inside chloroplast. At least, we know the framework of its action and function. Parallelly important, yet relatively unknown processes are carbon fixation taking place in deep-sea hydrothermal environments, which contain low levels or no solar radiation. In such environments, nature has to develop the systems to harvest geochemical and geothermal energy to generate high-energy electrons needed for carbon fixation. Yet, how nature utilizes temperature and chemical gradient fostered by geological settings remains largely unknown. In this talk, based on our findings of electrical current generation across a black smoker hydrothermal vent,[1,2] together with thermoelectrical conversion by deep-sea minerals,[3] I provide the new energetic underpinning of carbon fixation: de-coupled electron and heat transfer at deep-sea hydrothermal vents [4,5]. As catalysis at the deep-sea vent may tightly link with the origin and evolution of life, I provide the perspective to predict the first engine that drives the life emergence and fosters life complexity. (1) R. Nakamura, et al. Angew. Chem. Int. Ed., 49, 7692 (2010). (2) M. Yamamoto, et al. Angew. Chem. Int. Ed., 52, 10758 (2013). (3) R. Ang, et al. Angew. Chem. Int. Ed., 54, 12909 (2015). (4) A. Yamaguchi, et al. Electrochim. Acta, 141, 311 (2014). (5) A. Yamaguchi, et al. Springer, Chapter 4.3.2. (2016).