Vesicomyid Clams Research Articles

Serpentinite‐hosted chemosynthetic community of South Chamorro Seamount, Mariana Forearc

AbstractDeep‐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, we revisited South Chamorro to characterise its biodiversity. We located two regions of chemosynthetic communities dominated by bathymodioline mussels, vesicomyid clams, and chaetopterid parchment worms: one on the northwestern flank (‘Fryer Site’) and one on the southern summit (‘Summit Site’). We sampled a total of 20 species including 13 molluscs, five annelids, and two crustaceans – all present on the more active Summit Site but only a subset being found at Fryer Site. A mussel bed surrounding the Fryer Site was drilled by the Ocean Drilling Program in 2001 resulting in six holes, the deepest being 266 m (Hole 1200C). Cuttings ~50 cm deep still cover an approximately 60 m radius around Hole 1200C even 22 years later, and there is no sign of recovery. Low geofluid supply in serpentinite‐hosted seamounts may not allow decadal recovery of animal colonies, unlike a previous drilling site in an Okinawa Trough vent.

Evolutionarily ancient deep‐water seep communities in the Eocene Tethys: examples from Buje (Croatia)

AbstractWe report a newly discovered hydrocarbon seep deposit from the Eocene bathyal flysch, exposed in the town of Buje in Istria, Croatia. Molecular fossils of methane‐oxidizing prokaryotes and abundant banded botryoidal cements indicate strong fluid flux at this site. We systematically describe the fauna of this and another seep deposit previously reported from Buje. The faunal assemblages are composed of eight species, these being an unidentified solemyid protobranch bivalve, the nuculid Nucula bowerbanki?, the nuculanid Nuculana? sp., the mytilid Brachidontes? amanoi sp. nov., the two thyasirids Channelaxinus dinaricus sp. nov. and Thyasira histriaensis sp. nov., the lucinid bivalve Amanocina bujensis sp. nov., and a possible provannid gastropod. The two assemblages are of low diversity (4 and 5 species, respectively), and are dominated by chemosymbiotic species whose occurrence is largely restricted to seeps. Despite their spatial and stratigraphic proximity, the two deposits share only a single species, Channelaxinus dinaricus, probably due to different fluid flux regimes at both seeps. The Buje seep assemblages are among the very few Late Cretaceous to Palaeogene chemosynthesis‐based faunal assemblages from the Tethys Ocean (the others being Late Cretaceous vent assemblages from Cyprus). From an evolutionary perspective, the Buje seep communities consist of genera with Mesozoic origins but lack Cenozoic novelties such as bathymodiolin mussels and vesicomyid clams, which are known from coeval deposits from the Pacific and dominate vents and seeps today. Thus, the Buje seep fauna support previous assertions that the Eocene Tethyan seep faunas preserved an ancient aspect, whereas evolutionary novelties arose in the Pacific.

Seascape ecology in the vicinity of a Blake Ridge cold seep

Systematic surveys of the distribution of epibenthic megafaunal species relative to one another and to environmental variables in the deep sea can lead to inferences and testable hypotheses regarding factors that influence their distributions. Here we use a seascape approach to provide insight into the character and spatial extent of the influence of a chemosynthetic seep on the distribution of epibenthic megafauna and the nature of transition zones (ecotones). Faunal distributions were determined from georeferenced images of the seabed collected during a systematic survey (~ 400 m x 400 m) by the Autonomous Underwater Vehicle Sentry in the vicinity of a newly discovered methane bubble plume on the Blake Ridge Diapir. The survey area was found to include both seep and non-seep habitats. The sphere of influence of seep productivity on the surrounding benthic megafaunal assemblage was limited—on the order of 10’s of meters—based on ecotone analysis. Small but detectable redox anomalies in the water column (5 m above bottom) in the study area occurred on a similar horizontal scale. Distributions of background megafaunal taxa were non-random for many morphotypes and included both positive and negative associations between morphotypes and the seep habitat. Subtle variations in depth (<6 m) correlated with distributions of seep-associated vesicomyid clams, which occupy shallow depressions in the seabed. The seep habitat itself, comprising a patchy mosaic of megafaunal sub-communities (e.g., clam bed, mussel bed, background soft-sediment bathyal taxa) and transition zones, was at least as diverse as the surrounding non-seep habitat and contributes seep endemic morphotypes to regional biodiversity. While seep productivity may support prey fields for deep-diving beaked whales, any relationship between the seeps and whale feeding areas remains intriguing speculation. Like many other regions of the deep sea, Blake Ridge South has accumulated marine litter, including litter likely originating from scientific endeavors. The suite of observations and analyses deployed here underscore the importance of seep habitats in enriching regional biodiversity, provide a glimpse of the non-random complexity of species distributions from a seascape perspective, and establish ecological baselines against which future studies may measure natural and anthropogenic changes in the seascape.

Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment.

Previous studies have deciphered the genomic basis of host-symbiont metabolic complementarity in vestimentiferans, bathymodioline mussels, vesicomyid clams and Alviniconcha snails, yet little is known about the chemosynthetic symbiosis in Thyasiridae-a family of Bivalvia regarded as an excellent model in chemosymbiosis research due to their wide distribution in both deep-sea and shallow-water habitats. We report the first circular thyasirid symbiont genome, named Candidatus Ruthturnera sp. Tsphm01, with a size of 1.53 Mb, 1521 coding genes and 100% completeness. Compared to its free-living relatives, Ca. Ruthturnera sp. Tsphm01 genome is reduced, lacking components for chemotaxis, citric acid cycle and de novo biosynthesis of small molecules (e.g. amino acids and cofactors), indicating it is likely an obligate intracellular symbiont. Nevertheless, the symbiont retains complete genomic components of sulphur oxidation and assimilation of inorganic carbon, and these systems were highly and actively expressed. Moreover, the symbiont appears well-adapted to anoxic environment, including capable of anaerobic respiration (i.e. reductions of DMSO and nitrate) and possession of a low oxygen-adapted type of cytochrome c oxidase. Analysis of the host transcriptome revealed its metabolic complementarity to the incomplete metabolic pathways of the symbiont and the acquisition of nutrients from the symbiont via phagocytosis and exosome. By providing the first complete genome of reduced size in a thyasirid symbiont, this study enhances our understanding of the diversity of symbiosis that has enabled bivalves to thrive in chemosynthetic habitats. The resources will be widely used in phylogenetic, geographic and evolutionary studies of chemosynthetic bacteria and bivalves.

Methane seep communities on the Koryak slope in the Bering Sea

Methane seep communities on the Koryak slope in the Bering Sea were discovered in 2018 during the 82nd cruise of the RV Akademik M.A. Lavrentyev using ROV Comanche 18. Methane seeps found between 400 m and 695 m depth are the northernmost chemosynthesis-based habitats (∼61°N) known to date in the Pacific. Macrofauna species composition and community structure of methane seep and background benthic communities were investigated at three depth horizons: 400–402 m, 417–429 m and 647–695 m.A total of 335 macrofaunal species were identified. At the depth 647–695 m the species richness in the methane seep communities was 265 species and 72 species in the background. The deepest seep communities were characterized by the highest species richness, relatively high evenness and strong variations in the composition and structure. At shallower depths the species richness was low: 33–34 species at methane seeps and 66–71 in the background. The methane seep communities at shallow depths showed relatively low evenness and low diversity of community structure. The highest species richness at the greatest depth can be related in part to increased habitat heterogeneity associated with carbonate crusts and vesicomyid clam beds occurring only at deeper methane seeps. The deepest methane seep communities were dominated by the chemosymbiotrophic pliocardiine Calyptogena pacifica; dominant in the background was the ophiuroid Ophiophthalmus normani. At shallower methane seeps only single specimens of C. pacifica were found. The shallower methane seeps were dominated by the background species despite numerous extensive bacterial mats and high potential toxicity of the environment. The seep community at 417–429 m was dominated by the echinoid Brisaster latifrons with population density on the bacterial mat four times higher than in the background. Four chemosymbiotrophic species were recorded at 647–695 m and only one was found at shallower depths. Potentially obligate to reducing habitats polychaetes of the genus Neosabellides and Ophryotrocha occurred in methane seep communities at all depths. Further geochemical, geological and microbiological studies are required to better characterize differences of methane seeps at different depths and reasons of these differences.

Methane seepage intensity distinguish microbial communities in sediments at the Mid-Okinawa Trough

Shallow methane/sulfate transition zones in cold seeps are hotspots to study microbially mediated geochemical cycles due to high methane fluxes. However, our knowledge about the microbial communities in remote seafloor cold seep ecosystems with different methane seepage intensity is still sparse due to the challenge for sampling and visual observations. In this work, three remotely operated vehicle (ROV) video-guided push sediment cores were sampled from cold seep fields with different methane seepage intensity (low-intensity seepage, R5-C1; moderate-intensity seepage, R6-C2; high-intensity seepage, R6-C3) at the western slope of Mid-Okinawa Trough (Mid-OT) and subjected to high throughput sequencing of 16S rRNA genes for bacteria and archaea. Vesicomyid clams and white microbial mats are visible by video at R6-C3 with methane bubbles. The high relative abundances of anaerobic methanotrophic archaea (ANME-1, -2, and -3), δ-Proteobacteriacea and Campylobacteria in R6-C3 indicated that the processes of anaerobic methane oxidation (AOM), sulfate reduction and sulfur oxidation might occur in this active seeping site. In contrast, Bathyarchaeia, Nitrosopumilales, Sphingomonadales, and Burkholderiales were enriched in bubble-free sites, which commonly involved in the degradation of organic compounds. Principal coordinate analysis showed that both bacterial and archaeal communities were clustered according to sampling sites, also indicating the impact of methane seepage intensity on microbial communities. The co-occurrence network analysis revealed that microbes at the site with high methane fluxes mainly cooperated with each other to sustain the ecosystems, whereas competition enhanced at sites with low methane fluxes. Detection of thermophiles Thermoanaerobaculia and Hydrothermarchaeota may indicate microbial transmission from nearby hydrothermal vents, suggesting potential interactions between cold seepage and hydrothermal vent ecosystems. These results expand our knowledge about the composition and distribution of bacteria and archaea with different methane seepage intensity in cold seep field at the Mid-OT, contributing to the ongoing efforts in understanding carbon cycling in the cold seep ecosystems.

Archives of short-term fluid flow dynamics and possible influence of human activities at methane seeps: Evidence from high-resolution element geochemistry of chemosynthetic bivalve shells

The natural dynamics of fluid flow at methane seeps and increasingly human activities influence the biogeochemistry of the microenvironment and further determine the activity of the chemosynthetic communities within these ecosystems. However, ways to reconstruct short-term fluid flow dynamics and to decipher the influence of scientific exploration at seeps are limited. In this study, we present high-resolution trace elements/Ca ratios (Li/Ca, Mg/Ca, Ti/Ca, Mn/Ca, Co/Ca, Cu/Ca, Zn/Ca, Sr/Ca, Zr/Ca, Mo/Ca, Ba/Ca, Th/Ca and U/Ca ratios) from the shells of two species of chemosymbiotic bivalves (the thiotrophic vesicomyid clam Archivesica marissinica and the methanotrophic mussel Gigantidas haimaensis) from the Haima cold seeps of the South China Sea. We found that the complex distribution patterns of some trace elements (Mg/Ca, Sr/Ca, Mo/Ca and U/Ca ratios) in G. haimaensis are largely controlled by mineral composition or age. The observation of Co/Ca and Ba/Ca ratios in both species indicate strong physiological and environmental control on the incorporation of trace elements during the biomineralization process. Besides, the distribution patterns of other trace elements provide information that can be used to discuss open issues such as the loss of trace elements after death of the bivalves, and the possible influence of human activities such as sediment disturbance. Overall, this study emphasizes the potential for using high-resolution element geochemistry of seep bivalve shells to reveal the physiological and environmental factors that control the growth of bivalves, and to elucidate the potential history of fluid discharge at cold seeps.

Deep-sea infauna with calcified exoskeletons imaged in situ using a new 3D acoustic coring system (A-core-2000)

The deep ocean is Earth’s largest habitable space inhabited by diverse benthic organisms. Infauna play crucial roles in shaping sedimentary structures, relocating organic matter, porewater chemistry, and hence biogeochemical cycles. However, the visualization and quantification of infauna in situ inside deep-sea sediment has been challenging, due to their sparse distribution and that deep-sea cameras do not visualize animals living below the sediment surface. Here, we newly developed a 3D acoustic “coring” system and applied it to visualize and detect burrowing bivalves in deep-sea sediments. The in situ acoustic observation was conducted at a dense colony of vesicomyid clams in a hydrocarbon seep in Sagami Bay, Japan, focusing on a patch of juvenile clams with a completely infaunal life style. We clearly observed strong backscatters from the top and lower edges of animals in our 3D acoustic data. At least 17 reflectors were identified in the survey area (625 cm2), interpreted to correspond to living clams. The estimated depths of the lower edge of clams ranged between 41 and 98 mm. The acoustic system presented here is effective for detecting and monitoring infauna with calcified exoskeletons. This novel tool will help us better assess and understand the distribution of deep-sea infauna, particularly those groups with hard exoskeletons, as well as biogeochemical cycles.

Community Characteristics and Genetic Diversity of Macrobenthos in Haima Cold Seep

Knowledge about community structure and genetic diversity can help assess the potential for change in the loss and restoration of biodiversity, thereby facilitating effective management and ecosystem protection. Macroinvertebrate communities are an important biotic component of deep sea cold seep ecosystems. As Haima cold seep is increasingly being assessed for its potential gas hydrate mineral wealth, knowledge of community characteristics and genetic diversity of macrobenthos is needed to anticipate the potential impacts on biodiversity. In this study, we examined species diversity and community structure at five sites in the Haima cold seep using a remote-operated vehicle (ROV) for in situ surveying. The results identified 12 macrobenthic species from 5 phyla and 12 families. The macrobenthos community could be divided into two communities (H1 and H2=mussel bed community, and H3 and H4= vesicomyid clams community) based on CLUSTER and NMDS analyses. Gigantidas haimaensis (Mollusca), Branchipolynoe pettiboneae (Annelida), and Histampica haimaensis (Echinodermata) were most dominant within their respective phyla, with values of the dominance of 0.160, 0.021 and 0.114, respectively. The genetic diversity of these three typical macrobenthic species in the Haima cold seep was evaluated using the mitochondrial cytochrome c oxidase subunit I (COI) gene, haplotype, and nucleotide diversity values were 0.651 to 0.912 and 0.00148 to 0.00812, respectively, representing high haplotype diversity but low nucleotide diversity. Finally, mitochondrial concatenated dataset (MCD) sequences from three mitochondrial genes (ATP6, COI, and NAD4) and 294,734 genome-wide single nucleotide polymorphisms (SNPs) from restriction site-associated DNA-sequencing (RAD-seq) data were obtained from 60 individuals from two sites (H1 and H2), providing deep insight into the genetic diversity and structure of G. haimaensis, the engineer species in Haima cold seep. No significant genetic differentiation between G. haimaensis in H1 and H2 was detected based on MCD sequences. Nevertheless, when using SNP datasets, a small but clear genetic subdivision between G. haimaensis in the two sites as revealed by STRUCTURE and principal component analysis (PCA). The results comprehensively illuminate macrobenthos biodiversity in the Haima cold seep ecosystem and provide a baseline against which population dynamics may be assessed in the future.

Molecular detection of a novel perkinsid associated with the deep-sea clam Phreagena okutanii.

Based on environmental DNA surveys, it is widely held that phylogenetically diverse protists exist in chemosynthetic ecosystems. However, knowledge regarding the protists associated with the endemic animals inhabiting these environments is still very limited. In the present study, utilizing polymerase chain reaction (PCR) techniques, we detected fragments of the small subunit ribosomal RNA (SSU rRNA) gene and the internal transcribed spacer (ITS) region of the ribosomal RNA genes from a particular protist in the gills of the vesicomyid clam Phreagena okutanii (formerly described as Calyptogena okutanii), a representative animal in chemosynthetic ecosystems. Based on the phylogeny of the SSU rRNA gene, the organism in question belongs to the genus Perkinsus, which is exclusively composed of protistan parasites infecting mollusks. Intriguingly, based on the ITS phylogeny, this protist was not related to any known Perkinsus species and was deeply branched within the radiation of this genus, thus represents an undescribed species. In addition, the protist detected by PCR was localized to the intercellular spaces in the gills of the host clam with fluorescence in situ hybridization. Although the ecological significance of this novel deep-sea perkinsid remains unclear, our present findings may provide important insights into the diversity of the genus Perkinsus.

Lipid Biomarker Patterns Reflect Nutritional Strategies of Seep-Dwelling Bivalves From the South China Sea

Invertebrates living at methane seeps such as mussels and clams gain nutrition through symbiosis with chemosynthetic, chiefly methanotrophic and thiotrophic bacteria. Lipid biomarkers, including their compound-specific carbon stable isotope compositions, extracted from the host tissues are predestined for deciphering the various sources of diets and the associations among varying environments, endosymbionts, and hosts. Here, we investigated lipid inventories of soft tissues of two bathymodiolin mussel species hosting aerobic methanotrophic bacteria (Gigantidas platifrons from Site F and Gigantidas haimaensis from Haima seeps), one bathymodiolin mussel with thiotrophic bacteria (Bathymodiolus aduloides from Haima seeps), and one vesicomyid clam (Archivesica marissinica from Haima seeps) from the South China Sea. The gills of mussels hosting methanotrophic symbionts were found to contain high amounts of lipids of aerobic methanotrophic bacteria, such as the 4,4-dimethyl lanosterol, and other 4-methyl sterols, and the type I methanotroph-specific monounsaturated fatty acids (MUFAs) C16:1ω9 and C16:1ω8. Production of methyl-sterols is favored over fatty acids at low oxygen concentrations, as demonstrated in culture experiments with Methylococcus capsulatus. Since lesser fatty acids and abundant sterols are found in G. haimaensis compared to G. platifrons, G. haimaensis apparently lived at very low oxygen levels. Extremely high levels of MUFAs C16:1ω7 and C18:1ω7 were found in gill tissue of both B. aduloides and the vesicomyid clam A. marissinica. Given the absence of ω8 fatty acids, both B. aduloides and the vesicomyid clam contain thiotrophic bacteria only. The occurrence of 13C-enriched 24-methylenecholesterol in B. aduloides indicates that the animal complemented its diet by filter-feeding (ca. 3% of the total sterol inventory) on photosynthetically derived carbon, whereas the majority of sterols are pointing to a diet relying on endosymbionts. Different types of 4-methyl sterols were observed between the thiotroph-containing mussel and methanotroph-containing mussels, suggesting different biosynthetic steps are present from lanosterol to cholesterol between animal hosts and aerobic methanotrophs. Among the four bivalve species, specific lipid biomarker patterns diagnostic for either the symbionts or the hosts yielded similar δ13C values in each species, indicating that the host obtained its nutrition either directly from the symbionts or derived at least most of its carbon in this way. The information derived from lipid biomarkers of bivalves and their corresponding symbionts in modern environments is vital to interpret data from the rock record, where most other methods to study microbial community composition are not applicable.

Divergent paths in the evolutionary history of maternally transmitted clam symbionts.

Vertical transmission of bacterial endosymbionts is accompanied by virtually irreversible gene loss that results in a progressive reduction in genome size. While the evolutionary processes of genome reduction have been well described in some terrestrial symbioses, they are less understood in marine systems where vertical transmission is rarely observed. The association between deep-sea vesicomyid clams and chemosynthetic Gammaproteobacteria is one example of maternally inherited symbioses in the ocean. Here, we assessed the contributions of drift, recombination and selection to genome evolution in two extant vesicomyid symbiont clades by comparing 15 representative symbiont genomes (1.017-1.586 Mb) to those of closely related bacteria and the hosts' mitochondria. Our analyses suggest that drift is a significant force driving genome evolution in vesicomyid symbionts, though selection and interspecific recombination appear to be critical for maintaining symbiont functional integrity and creating divergent patterns of gene conservation. Notably, the two symbiont clades possess putative functional differences in sulfide physiology, anaerobic respiration and dependency on environmental vitamin B12, which probably reflect adaptations to different ecological habitats available to each symbiont group. Overall, these results contribute to our understanding of the eco-evolutionary processes shaping reductive genome evolution in vertically transmitted symbioses.

Macrofaunal Distribution, Diversity, and Its Ecological Interaction at the Cold Seep Site of Krishna-Godavari Basin, East Coast of India.

Cold seeps are characterized by typical endemic communities with associated microorganisms that depend on sulfide, methane, reduced nitrogenous compounds, and metals as electron donors for their survival through chemosynthesis. The discovery of an active cold seep site in January 2018 in the Krishna-Godavari (K-G) basin of Bay of Bengal was followed by a transit cruise in March 2018 to investigate the distribution and diversity of macrofauna. Further, the ambient sediment and pore water biochemistry were estimated to understand its relationship with macrofauna and the microbial associates of the sediment. Samples were collected at a water depth of around 1750m at 3 stations: SP1, SP2, and SP3, using the box corer. The benthic fauna at the sites consisted mainly of Bivalvia, shrimps of Caridea family, Gastropoda species, Malacostraca species, Polychaeta, and few species of Echinoidea, Ophiuroidea, and Echiura. A total of 2313 macrofaunal individuals belonging to 8 classes, 18 families, and 20 species were identified from all the three stations. The communities were diverse at these sites with an average Shannon diversity index of 1.64 and are closely related to the lineages previously studied in ecologically similar environments. Most of the macrofauna were found to be filter feeders preferring a low organic carbon environment. Relict vesicomyid clams at the present study site suggest the succession from vesicomyids to the present composition of bivalve mussels and siboglinid worms. The microbial associates in the sediment significantly correlated with methane and hydrogen sulfide concentrations. The study suggests that the K-G basin cold seep serves as a conducive environment for the flourishing of benthic communities and therefore can support a rich biodiversity.

Possible Roles of Hypotaurine and Thiotaurine in the Vesicomyid Clam Phreagena okutanii.

AbstractVesicomyid clams, which inhabit deep-sea hydrothermal vents and hydrocarbon seeps, are nutritionally dependent on symbiotic, chemoautotrophic bacteria that produce organic matter by using hydrogen sulfide. Vesicomyid clams absorb hydrogen sulfide from the foot and transport it in their hemolymph to symbionts in the gill. However, mechanisms to cope with hydrogen sulfide toxicity are not fully understood. Previous studies on vent-specific invertebrates, including bathymodiolin mussels, suggest that hypotaurine, a precursor of taurine, mitigates hydrogen sulfide toxicity by binding it to bisulfide ion, so as to synthesize thiotaurine. In this study, we cloned cDNAs from the vesicomyid clam Phreagena okutanii for the taurine transporter that transports hypotaurine into cells and for cysteine dioxygenase and cysteine-sulfinate decarboxylase, major enzymes involved in hypotaurine synthesis. Results of reverse-transcription polymerase chain reaction indicate that mRNAs of these three genes are most abundant in the foot, followed by the gill. However, hypotaurine and thiotaurine levels, measured by reverse-phase high-performance liquid chromatography, were low in the foot and high in the gill. In addition, thiotaurine was detected in hemolymph cells. Hypotaurine synthesized in the foot may be transported to the gill after binding to bisulfide ion, possibly by hemolymph cells.

Hydrothermal Activity at a Cretaceous Seamount, Canary Archipelago, Caused by Rejuvenated Volcanism

Our knowledge of venting at intraplate seamounts is limited. Almost nothing is known about past hydrothermal activity at seamounts, because indicators are soon blanketed by sediment. This study provides evidence for temporary hydrothermal circulation at Henry Seamount, a re-activated Cretaceous volcano near El Hierro island, close to the current locus of the Canary Island hotspot. In the summit area at around 3000–3200 m water depth, we found areas with dense coverage by shell fragments from vesicomyid clams, a few living chemosymbiotic bivalves, and evidence for sites of weak fluid venting. Our observations suggest pulses of hydrothermal activity since some thousands or tens of thousands years, which is now waning. We also recovered glassy heterolithologic tephra and dispersed basaltic rock fragments from the summit area. Their freshness suggests eruption during the Pleistocene to Holocene, implying minor rejuvenated volcanism at Henry Seamount probably related to the nearby Canary hotspot. Heat flow values determined on the surrounding seafloor (49 ± 7 mW/m2) are close to the expected background for conductively cooled 155 Ma old crust; the proximity to the hotspot did not result in elevated basal heat flow. A weak increase in heat flow toward the southwestern seamount flank likely reflects recent local fluid circulation. We propose that hydrothermal circulation at Henry Seamount was, and still is, driven by heat pulses from weak rejuvenated volcanic activity. Our results suggest that even single eruptions at submarine intraplate volcanoes may give rise to ephemeral hydrothermal systems and generate potentially habitable environments.

The Diversity, Composition, and Putative Functions of Gill-Associated Bacteria of Bathymodiolin Mussel and Vesicomyid Clam from Haima Cold Seep, South China Sea.

The Haima cold seep, which is one of the two active cold seeps in the South China Sea, is known for its great ecological importance. The seep bivalves are assumed to depend mainly on their bacterial symbiosis for survival and growth. However, information on the bacterial diversity, composition, and putative function of gill-associated of dominant dwelling animals in Haima cold seep remain elusive. Herein, we adopted a high-throughput sequencing of 16S rRNA gene amplicons, and function prediction methods (Functional Annotation of Prokaryotic Taxa (FAPROTAX) and Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICURUSTs)) to purposely illustrate the taxonomic and phylogenetic diversity, composition, and putative functions of the symbionts in bathymodiolin mussel Gigantidas haimaensis (Bivalvia: Mytilidae: Gigantidas) and vesicomyid clam Archivesica marissinica (Bivalvia: Glossoidea: Vesicomyidae). The predominant microbes of both species were Proteobacteria and Gammaproteobacteria on the phylum and class level, respectively. The taxonomic and phylogenetic diversity of gill microbial communities in G. haimaensis were significantly different from those in A. marissinica (p < 0.05). Nine functional groups, including seven carbon-related biogeochemical groups, were identified through the FAPROTAX analysis. However, the most dominant groups for G. haimaensis and A. marissinica were both chemoheterotrophic. G. haimaensis and A. marissinica shared many pathways, however, 16 obtained Kyoto Encyclopedia of Genes and Genomes (KEGG) orthologous groups (42.11%) significantly differed between the two species (p < 0.05). These findings would provide insight into the functions of microbes in the element cycling and energy flow as well as the host-symbiont relationship of bivalves in the Haima cold seep environment.

Host-Endosymbiont Genome Integration in a Deep-Sea Chemosymbiotic Clam.

Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.

Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing

Abstract In deep-sea hydrothermal vents and hydrocarbon seeps, chemoautotrophic bacteria use chemical substances as energy resources for primary production, ultimately supporting dense communities of megafauna, including the charismatic giant vesicomyid clams. These clams inherit their endosymbionts from their parents and house them intracellularly in their gills. How these organisms maintain their unique symbiotic relationship at the cellular level, however, remains largely unclear. In the present study, the transcriptomes of different organs in Phreagena okutanii collected from a hydrothermal vent and in Archivesica marissinica collected from a methane seep were sequenced in order to decipher their host-symbiont relationships. Expressional analyses of the transcriptomes showed that the tricarboxylic acid (TCA) cycle-related genes, the Rab gene family, and the lysozyme genes were highly expressed in the gills. Furthermore, genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism were positively selected. The endosymbiont genes involved in sulfur oxidation, oxidative phosphorylation, and adenosine triphosphate (ATP) synthesis were highly expressed. The results suggest that the vesicomyid clams provide intermediates to fulfill the metabolic needs of their endosymbionts, and in return the endosymbionts actively generate nutrients for the hosts through being digested by the lysozymes of the host. Furthermore, the positive selection of genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism indicates the molecular adaptation of the host in order to benefit from symbiosis. Overall, the present study provides the first set of transcriptomes for deep-sea chemosymbiotic vesicomyid clams, facilitating a better understanding of the host-symbiont relationship that has allowed them to become dominant animals in deep-sea hydrothermal vents and cold seeps.

Fauna of the Kemp Caldera and its upper bathyal hydrothermal vents (South Sandwich Arc, Antarctica).

Faunal assemblages at hydrothermal vents associated with island-arc volcanism are less well known than those at vents on mid-ocean ridges and back-arc spreading centres. This study characterizes chemosynthetic biotopes at active hydrothermal vents discovered at the Kemp Caldera in the South Sandwich Arc. The caldera hosts sulfur and anhydrite vent chimneys in 1375–1487 m depth, which emit sulfide-rich fluids with temperatures up to 212°C, and the microbial community of water samples in the buoyant plume rising from the vents was dominated by sulfur-oxidizing Gammaproteobacteria. A total of 12 macro- and megafaunal taxa depending on hydrothermal activity were collected in these biotopes, of which seven species were known from the East Scotia Ridge (ESR) vents and three species from vents outside the Southern Ocean. Faunal assemblages were dominated by large vesicomyid clams, actinostolid anemones, Sericosura sea spiders and lepetodrilid and cocculinid limpets, but several taxa abundant at nearby ESR hydrothermal vents were rare such as the stalked barnacle Neolepas scotiaensis. Multivariate analysis of fauna at Kemp Caldera and vents in neighbouring areas indicated that the Kemp Caldera is most similar to vent fields in the previously established Southern Ocean vent biogeographic province, showing that the species composition at island-arc hydrothermal vents can be distinct from nearby seafloor-spreading systems. δ13C and δ15N isotope values of megafaunal species analysed from the Kemp Caldera were similar to those of the same or related species at other vent fields, but none of the fauna sampled at Kemp Caldera had δ13C values, indicating nutritional dependence on Epsilonproteobacteria, unlike fauna at other island-arc hydrothermal vents.

Host hybridization as a potential mechanism of lateral symbiont transfer in deep-sea vesicomyid clams.

Deep‐sea vesicomyid clams live in mutualistic symbiosis with chemosynthetic bacteria that are inherited through the maternal germ line. On evolutionary timescales, strictly vertical transmission should lead to cospeciation of host mitochondrial and symbiont lineages; nonetheless, examples of incongruent phylogenies have been reported, suggesting that symbionts are occasionally horizontally transmitted between host species. The current paradigm for vesicomyid clams holds that direct transfers cause host shifts or mixtures of symbionts. An alternative hypothesis suggests that hybridization between host species might explain symbiont transfers. Two clam species, Archivesica gigas and Phreagena soyoae, frequently co‐occur at deep‐sea hydrocarbon seeps in the eastern Pacific Ocean. Although the two species typically host gammaproteobacterial symbiont lineages marked by divergent 16S rRNA phylotypes, we identified a number of clams with the A. gigas mitotype that hosted symbionts with the P. soyoae phylotype. Demographic inference models based on genome‐wide SNP data and three Sanger sequenced gene markers provided evidence that A. gigas and P. soyoae hybridized in the past, supporting the hypothesis that hybridization might be a viable mechanism of interspecific symbiont transfer. These findings provide new perspectives on the evolution of vertically transmitted symbionts and their hosts in deep‐sea chemosynthetic environments.