Chemosynthetic Habitats Research Articles

Metabolically-versatile Ca. Thiodiazotropha symbionts of the deep-sea lucinid clam Lucinoma kazani have the genetic potential to fix nitrogen.

Lucinid clams are one of the most diverse and widespread symbiont-bearing animal groups in both shallow and deep-sea chemosynthetic habitats. Lucinids harbor Ca. Thiodiazotropha symbionts that can oxidize inorganic and organic substrates such as hydrogen sulfide and formate to gain energy. The interplay between these key metabolic functions, nutrient uptake and biotic interactions in Ca. Thiodiazotropha is not fully understood. We collected Lucinoma kazani individuals from next to a deep-sea brine pool in the eastern Mediterranean Sea, at a depth of 1150m and used Oxford Nanopore and Illumina sequencing to obtain high-quality genomes of their Ca. Thiodiazotropha gloverae symbiont. The genomes served as the basis for transcriptomic and proteomic analyses to characterize the in situ gene expression, metabolism and physiology of the symbionts. We found genes needed for N2 fixation in the deep-sea symbiont's genome, which, to date, were only found in shallow-water Ca. Thiodiazotropha. However, we did not detect the expression of these genes and thus the potential role of nitrogen fixation in this symbiosis remains to be determined. We also found the high expression of carbon fixation and sulfur oxidation genes, which indicate chemolithoautotrophy as the key physiology of Ca. Thiodiazotropha. However, we also detected the expression of pathways for using methanol and formate as energy sources. Our findings highlight the key traits these microbes maintain to support the nutrition of their hosts and interact with them.

Genetic connectivity and isotopic niches of alvinocaridid shrimps from chemosynthetic habitats in Aotearoa/New Zealand, with a new Alvinocaris species

Genetic connectivity and isotopic niches of alvinocaridid shrimps from chemosynthetic habitats in Aotearoa/New Zealand, with a new Alvinocaris species

Biogeography and depth partitioning in deep‐sea gastropods at the Pacific Costa Rica Margin

AbstractAimUnderstanding the global distribution of biodiversity and the factors that influence it are among the central goals of biogeography. How abiotic and biotic factors limit species' ranges has been investigated across a variety of environments and taxonomic groups. However, such investigations across oceanic depths remain underrepresented, particularly for chemosynthetic environments such as hydrocarbon seeps. The depth differentiation (DD) hypothesis suggests that steep environmental gradients in the upper depths of the ocean may limit species' ranges over relatively short vertical distances. The present study aims to investigate the evidence for the DD hypothesis at hydrocarbon seep sites along the Pacific Costa Rica Margin (CRM) by investigating the biogeographic distributions of gastropods sampled there and the factors that influence them.LocationCosta Rica.TaxonMollusca, Gastropoda, Provannidae, Genus: Provanna (Dall, 1918).Methods1813 Provanna snails were collected across 1300 metres (m) of depth from Costa Rican hydrocarbon seeps. To test the DD hypothesis, species partitioning across the depth range was investigated. In addition to gradients in oceanographic conditions, such as temperature, oxygen, and salinity, other factors potentially responsible for filtering species were also considered as alternative hypotheses, including the availability of biogenic substrate, the availability of and reliance on chemosynthetic fluids, and specific preferences for certain environmental conditions.Results and Main ConclusionsThree species of Provanna were identified from the CRM and exhibited partitioning across depth. For the two dominant species (P. laevis and P. goniata), the data suggest that depth‐associated oceanographic conditions are more likely than any other factor investigated to explain their observed partitioning across depth, supporting the DD hypothesis. This study also presents novel evidence that such partitioning may be unilaterally determined, wherein species with narrower depth ranges may limit the local depth ranges of others. This study represents an extension of biogeographic range limit literature into chemosynthetic habitats and across oceanic depths.

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 supply drives prokaryotic community assembly and networks at cold seeps of the South China Sea.

Marine cold seeps are unique chemosynthetic habitats fuelled by deeply sourced hydrocarbon-rich fluids discharged at the seafloor. Through oxidizing methane and other hydrocarbons, microorganisms inhabiting cold seeps supply subsurface-derived energy to higher trophic levels, sustaining highly productive oases of life in the deep sea. Despite the central role of microbiota in mediating biogeochemical cycles, the factors that govern the assembly and network of prokaryotic communities in cold seeps remain poorly understood. Here we analysed the geochemical and microbiological profiles of 11 different sediment cores from two spatially distant cold seeps of the South China Sea. We show that prokaryotic communities belonging to the same methane-supply regimes (high-methane-supply, low-methane-supply and non-seep control sediments) had a highly similar community structure, regardless of geographical location, seep-associated biota (mussel, clam, microbial mat) and sediment depth. Methane supply appeared to drive the niche partitioning of anaerobic methanotrophic archaea (ANME) at the regional scale, with ANME-1 accounting for >60% sequence abundance of ANME in the high-methane-supply sediments, while ANME-2 dominated (>90%) the low-methane-supply sediments. Increasing methane supply enhanced the contribution of environmental selection but lessened the contributions of dispersal limitation and drift to overall community assembly. High methane supply, moreover, promoted a more tightly connected, less stable prokaryotic network dominated by positive correlations. Together, these results provide a potentially new framework for understanding the niches and network interplay of prokaryotic communities across different methane seepage regimes in cold-seep sediments.

New species of Ophryotrocha (Annelida: Dorvilleidae) associated with deep-sea reducing habitats in the Bering Sea, Northwest Pacific

Four species of Ophryotrocha (Annelida, Dorvilleidae) from deep-sea reducing habitats (methane seeps on the Koryak slope and hydrothermal vents of the submarine Piip Volcano) were collected in the western part of the Bering Sea, NW Pacific. Descriptions of two of these new Ophryotrocha species, namely O. beringiana sp. nov. and O. seepens sp. nov., confirmed with molecular analyses, are presented herein. The detailed descriptions with electron microscopy illustrations for the new species are presented and their differences from similar species are discussed. In addition to the morphological description, the phylogenetic relationships of the new dorvilleids are provided using two nuclear (18S RNA, histone H3) and two mitochondrial (16S RNA and cytochrome c oxidase subunit 1, COI) markers in an analysis containing 54 terminal taxa. Phylogenetic analyses using MrBayes and Maximum Likelihood analyses show that O. beringiana sp. nov. and O. seepens sp. nov. are sister species, and together with O. platykephale, O. globopalpata and O. flabella form a subclade of deep-sea Pacific species within a clade referred to here as ‘globopalpata–platykephale’. In our molecular analysis, the clade currently consists of ten species, nine of those (except for O. longidentata, the only shallow Atlantic species not reported in chemosynthetic habitats) have been described from Pacific deep-sea reducing environments (hydrothermal vents, cold methane seeps, whale-falls). The ecology and geographic distribution of the reported species are discussed.

Phylogenetic placement, morphology and gill-associated bacteria of a new genus and species of deep-sea mussel (Mytilidae: Bathymodiolinae) from the South China Sea

Mussels in the subfamily Bathymodiolinae are common inhabitants of deep-sea chemosynthetic habitats, but in many places their diversity remains unknown. Here we describe Nypamodiolus samadiae n. gen. et n. sp. (Mytilidae: Bathymodiolinae) based on samples collected from the Haima cold seep in the South China Sea. Phylogenetic analyses based on fragments of three mitochondrial (cox1, 16S rRNA and nad4) and three nuclear (18S rRNA, 28S rRNA and histone H3) genes show that this new species belongs to a new genus, Nypamodiolus, which includes three named species (Myrina longissima Thiele and Jaeckel, 1931, Myrina simpsoni Marshall, 1900, Idasola japonica Habe, 1976) and a few undescribed species. Nypamodiolus n. gen. is characterized by small-sized, modioliform to fan-shaped shells with the umbones in a non-terminal position, and by robust anterior and posterior byssal retractor muscles arranged in roughly one plane. Most closely related to Nypamodiolus samadiae n. sp. is an undescribed species from the northern Papua New Guinea, to which it has a Kimura-2-parameter genetic distance of 11.8% for cox1. Sequencing the V3–V4 region of the microbial 16S rRNA gene reveals two dominant gill-associated bacteria in the new species, including one sulfur-oxidizing Gammaproteobacteria (relative abundance: 43.8–58.8%) and one unclassified Spirochaetes (relative abundance: 23.9–28.1%). Morphologically, N. samadiae n. sp. is similar to N. simpsoni, while can be distinguished by a larger maximum shell size (45.0 mm vs. 40.0 mm), larger length/height ratio (2.6–2.9 vs. 2.1–2.4), broader posterior end, slightly curved dorsal margin, and more anterior umbones.

Phylogeny and adaptative evolution to chemosynthetic habitat in barnacle (Cirripedia: Thoracica) revealed by mitogenomes

Thoracican barnacles represent a unique group that has evolved in parallel identical somatotype s (sessile, stalked and asymmetric) in both normal and chemosynthetic environments. Hydrothermal vents and methane seeps are typical extreme deep-sea chemosynthetic habitats for marine macrobenthos. Characterizing the evolutionary history and adaptive strategy of barnacles is fundamentally important for understanding their origin, speciation, and diversification. Herein, we performed a series of phylogenetic analyses focusing on the mitochondrial genomes of the main extant barnacle lineages. Phylogenetic inferences and topology tests contradict the view of the sister relationship between verrucomorphs and balanomorphs, instead revealing that pollicipedids, calanticids and balanomorphs share common ancestor. Selective pressure analyses indicate that the two barnacle lineages of chemosynthetic ecosystems exhibit similar patterns in their evolution of adaptive characters, but have diverse and specific positive substitution sites of mitogenomes. Divergence times suggest that chemosynthetic barnacles originated in the Cenozoic, coinciding with the origins of other metazoan animals in chemosynthetic habitats as well as the Paleogene mass extinction and oceanic anoxic events. It is reasonable to suppose that ecological niche vacancy, sitotaxis, gene specificity in adaptive stress responses, and the subdivision of the ecological niche contributed to the origin and diversification of barnacles in chemosynthetic ecosystems.

Some Biogeochemical Characteristics of the Trace Element Bioaccumulation in the Benthic Fauna of the Piip Volcano (The Southwestern Bering Sea)

The Piip Volcano is a submarine volcanic edifice occupying the central part of the Volcanologists Massif in the southwestern Bering Sea, with two tops, southern and northern. The minimum depth of the northern top is located at 368 m, and of the southern at 464 m. Active hydrothermal venting occurring at both summits of the volcano supports diverse biological communities, including animals specific for chemosynthetic habitats. In benthic organisms inhabiting the northern and southern tops of the Piip Volcano, for the first time, we examined distribution patterns of the following trace elements: titanium, vanadium, chromium, manganese, iron, nickel, copper, zinc, arsenic, selenium, zirconium, molybdenum, silver, cadmium, antimony, barium, tungsten, lead, bismuth, and uranium. The element contents were quantified by the ICP-MS. Total carbon (TC) and total inorganic carbon (TIC) were determined using a Shimadzu TOC-L-CPN and mineral composition of sediment was determined using the XRD. In the water of the biotope from the northern top, concentrations of Mn, Zn, Ag, Cd, Sb, W, Pb were 2–6 times, and Ba was 50 times higher than those from the southern top. This was attributed to the lower temperature of fluids emanating at the southern top. An abundant population of Calyptogena pacifica (Bivalvia: Vesicomyidae: Pliocardiinae) was found only at the southern top. The main target of most trace elements, such as Fe, V, Cr, Co, Ni, Zn, As, Mo, Ag, Cd, W, Pb, Bi, and U were the soft parts of Calyptogena pacifica (with high TOC content, on average 53.1% in gills and 49.6% in the rest of the body). Gills were characterized by particular high contents (>100 µg g−1 dry w.) of Zn, Cd, Fe, Ni, Cu, and Pb, which can form sulphides or be associated with them. Shells of C. pacifica, as well as Brachiopoda, were depleted in these elements, as well as tissues of the carnivores Paguridae (Crustacea) and Actiniaria (Anthozoa). In suspension feeders from both tops, the lower contents of most elements were detected. Estimation of Biological Concentration Factor (BCF) for most elements varied from 102 to 104, reaching n105 for Ni, Zn, Ag, Cd, and Pb. A significant difference in BCF values between Fe and Mn was revealed.

Description of a new species of Histampica (Ophiuroidea: Ophiothamnidae) from cold seeps in the South China Sea and analysis of its mitochondrial genome

Ophiuroids are widely distributed marine benthic organisms, but very few species of ophiuroids have been reported from deep-sea chemosynthetic habitats including hydrothermal vents and cold seeps. In this study, a new species of Ophiothamnidae, Histampica haimaensis sp. nov., collected from cold seeps in the South China Sea, was described based on morphological and genetic analyses. The new species, representing the first known occurrence of Histampica from chemosynthetic habitats, is distinct from its congeners in having long triangular or half elliptical radial shields that are not in contact with each other, four stout, tapering and blunt arm spines, and three or four lateral oral papillae on each side of the jaw, including distally two large and broad papillae and proximally one or two small and narrow papillae. Phylogenetic analysis based on mitochondrial COX1 gene supports the morphological identification. A complete mitochondrial genome (mtgenome) of the new species was characterized by genome skimming. It is 15,759 base pairs in length and contains 37 genes including 13 protein coding genes, two ribosomal RNA genes and 22 transfer RNA (tRNA) genes. Among the tRNA genes, trnL and trnS are duplicated. When compared with the mtgenomes from the same family of ophiuroids, the mtgenome of H. haimaensis sp. nov. has undergone four potential historical gene order reversals, and one tandem duplication random loss event. ND1, ND2 and ND5 each contains a positively selected site, while COX2 contains three positively selected sites This study provides morphological description to H. haimaensis sp. nov. and reports the first cold-seep ophiuroid mitochondrial genome with a novel gene order arrangement and signals of positive selection, which may have contributed to adaption of Ophiuroidea to the deep-sea chemosynthetic environments.

Chiridota heheva\u2014the cosmopolitan holothurian

Chemosynthetic ecosystems have long been acknowledged as key areas of enrichment for deep-sea life, supporting hundreds of endemic species. Echinoderms are among the most common taxa inhabiting the periphery of chemosynthetic environments, and of these, chiridotid holothurians are often the most frequently observed. Yet, published records of chiridotids in these habitats are often noted only as supplemental information to larger ecological studies and several remain taxonomically unverified. This study therefore aimed to collate and review all known records attributed to Chiridota Eschscholtz, 1829, and to conduct the first phylogenetic analysis into the relationship of these chiridotid holothurians across global chemosynthetic habitats. We show that Chiridota heheva Pawson & Vance, 2004 is a globally widespread, cosmopolitan holothurian that occupies all three types of deep-sea chemosynthetic ecosystem—hydrothermal vents, cold seeps and organic falls—as an organic-enrichment opportunist. Furthermore, we hypothesise that C. heheva may be synonymous with another vent-endemic chiridotid, Chiridota hydrothermica Smirnov et al., 2000, owing to the strong morphological, ecological and biogeographical parallels between the two species, and predict that any chiridotid holothurians subsequently discovered at global reducing environments will belong to this novel species complex. This study highlights the importance of understudied, peripheral taxa, such as holothurians, to provide insights to biogeography, connectivity and speciation at insular deep-sea habitats.

Molecular affinity of Southwest Atlantic Alvinocaris muricola with Atlantic Equatorial Belt populations

Specialist fauna populations from chemosynthetic ecosystems are connected through larval stages travelling in current highways in the vast deep sea. One shrimp family of such specialists, Alvinocarididae, is hitherto known to be endemic to vents and seeps with no reported occurrence in ephemeral organic-rich chemosynthetic habitats. Here we report the first occurrence of Alvinocaris muricola on experimentally deployed whale bones and wood parcels in the Brazil margin (21° to 26°S) at 1500 and 3300 m depth. We sequenced the COI, 16S and 28S markers for molecular identification of Southwest Atlantic (SWAtl) specimens and used COI sequences to inspect the molecular diversity and genetic distance between the SWAtl and the Atlantic Equatorial Belt (AEB) populations. SWAtl A. muricola exhibited lower nucleotide and haplotype diversities in comparison with populations along the AEB. The low genetic divergence detected here between the SWAtl and AEB populations is likely a result of larval connectivity through equatorial currents from the East Atlantic margin populations, whereas the SWAtl may be supplied through western boundary currents at bathypelagic depths. The occurrence of A. muricola in organic falls suggests the existence of other deep-sea chemosynthesis-based ecosystems in the SWAtl that could function as larval sources to organic islands and vice versa. Our study additionally supports the ecological stepping-stone role of organic falls between vent and seep ecosystems.

From wood to vent: first cocculinid limpet associated with hydrothermal activity discovered in the Weddell Sea

AbstractLush ‘oases’ of life seen in chemosynthetic ecosystems such as hot vents and cold seeps represent rare, localized exceptions to the generally oligotrophic deep ocean floor. Organic falls, best known from sunken wood and whale carcasses, are additional sources of such oases. Kemp Caldera (59°42'S, 28°20'W) in the Weddell Sea exhibits active hydrothermal vents and a natural whale fall in close proximity, where an undescribed cocculinid limpet was found living in both types of chemosynthetic habitats. This represents the first member of the gastropod order Cocculinida discovered from hot vents, and also the first record from the Southern Ocean. Here, we applied an integrative taxonomy framework incorporating traditional dissection, electron microscopy, genetic sequencing and 3D anatomical reconstruction through synchrotron computed tomography in order to characterize this species. Together, our data revealed an unusual member of the genusCocculinawith a highly modified radula for feeding on bacterial film, described herein asCocculina enigmadontan. sp. Its phylogenetically derived position within the largely wood-inhabitingCocculinaindicates that it probably evolved from an ancestor adapted to living on sunken wood, providing a compelling case of the ‘stepping stone’ evolutionary trajectory from organic falls to seeps and vents.

Intra-host symbiont diversity in eastern Pacific cold seep tubeworms identified by the 16S-V6 region, but undetected by the 16S-V4 region.

Vestimentiferan tubeworms are key taxa in deep-sea chemosynthetic habitats worldwide. As adults they obtain their nutrition through their sulfide-oxidizing bacterial endosymbionts, which are acquired from the environment. Although horizontal transmission should favor infections by various symbiotic microbes, the current paradigm holds that every tubeworm harbors only one endosymbiotic 16S rRNA phylotype. Although previous studies based on traditional Sanger sequencing have questioned these findings, population level high-throughput analyses of the symbiont 16S diversity are still missing. To get further insights into the symbiont genetic variation and uncover hitherto hidden diversity we applied state-of-the-art 16S-V4 amplicon sequencing to populations of the co-occurring tubeworm species Lamellibrachia barhami and Escarpia spicata that were collected during E/V Nautilus and R/V Western Flyer cruises to cold seeps in the eastern Pacific Ocean. In agreement with earlier work our sequence data indicated that L. barhami and E. spicata share one monomorphic symbiont phylotype. However, complementary CARD-FISH analyses targeting the 16S-V6 region implied the existence of an additional phylotype in L. barhami. Our results suggest that the V4 region might not be sufficiently variable to investigate diversity in the intra-host symbiont population at least in the analyzed sample set. This is an important finding given that this region has become the standard molecular marker for high-throughput microbiome analyses. Further metagenomic research will be necessary to solve these issues and to uncover symbiont diversity that is hidden below the 16S rRNA level.

Phylogeny, biogeography and systematics of Pacific vent, methane seep, and whale-fall Parougia (Dorvilleidae : Annelida), with eight new species

Dorvilleidae is a diverse group of annelids found in many marine environments and also commonly associated with chemosynthetic habitats. One dorvilleid genus, Parougia, currently has 11 described species, of which two are found at vents or seeps: Parougia wolfi and Parougia oregonensis. Eight new Parougia species are recognised and described in this study from collections in the Pacific Ocean, all from whale-falls, hydrothermal vents, or methane seeps at ~600-m depth or greater. The specimens were studied using morphology and phylogenetic analyses of DNA sequences from mitochondrial (cytochrome c oxidase subunit I, 16S rRNA, and cytochrome b) and nuclear (18S rRNA and histone 3) genes. Six sympatric Parougia spp. were found at Hydrate Ridge, Oregon, while three of the Parougia species occurred at different types of chemosynthetic habitats. Two new species were found over wide geographical and bathymetric ranges. Another dorvilleid genus, Ophryotrocha, has previously been highlighted as diversifying in the deep-sea environment. Our results document the hitherto unknown diversity of another dorvilleid genus, Parougia, at various chemosynthetic environments. http://zoobank.org/urn:lsid:zoobank.org:pub:EC7EBBEA-2FB5-43D6-BE53-1A468B541A5C

Discriminative biogeochemical signatures of methanotrophs in different chemosynthetic habitats at an active mud volcano in the Canadian Beaufort Sea

Several mud volcanoes are active in the Canadian Beaufort Sea. In this study, we investigated vertical variations in methanotrophic communities in sediments of the mud volcano MV420 (420 m water depth) by analyzing geochemical properties, microbial lipids, and nucleic acid signatures. Three push cores were collected with a remotely operated vehicle from visually discriminative habitats that were devoid of megafauna and/microbial mats (DM) to the naked eye, covered with bacterial mats (BM), or colonized by siboglinid tubeworms (ST). All MV420 sites showed the presence of aerobic methane oxidation (MOx)- and anaerobic methane oxidation (AOM)-related lipid biomarkers (4α-methyl sterols and sn-2-hydroxyarchaeol, respectively), which were distinctly different in comparison with a reference site at which these compounds were not detected. Lipid biomarker results were in close agreement with 16S rRNA analyses, which revealed the presence of MOx-related bacteria (Methylococcales) and AOM-related archaea (ANME-2 and ANME-3) at the MV420 sites. 4α-methyl sterols derived from Methylococcales predominated in the surface layer at the BM site, which showed a moderate methane flux (0.04 mmol cm−2 y−1), while their occurrence was limited at the DM (0.06 mmol cm−2 y−1) and ST (0.01 mmol cm−2 y−1) sites. On the other hand, 13C-depleted sn-2-hydroxyarchaeol potentially derived from ANME-2 and/or ANME-3 was abundant in down-core sediments at the ST site. Our study indicates that a niche diversification within this mud volcano system has shaped distinct methanotrophic communities due to availability of electron acceptors in association with varying degrees of methane flux and bioirrigation activity.

Molecular characterization of Bathymodiolus mussels and gill symbionts associated with chemosynthetic habitats from the U.S. Atlantic margin.

Mussels of the genus Bathymodiolus are among the most widespread colonizers of hydrothermal vent and cold seep environments, sustained by endosymbiosis with chemosynthetic bacteria. Presumed species of Bathymodiolus are abundant at newly discovered cold seeps on the Mid-Atlantic continental slope, however morphological taxonomy is challenging, and their phylogenetic affinities remain unestablished. Here we used mitochondrial sequence to classify species found at three seep sites (Baltimore Canyon seep (BCS; ~400m); Norfolk Canyon seep (NCS; ~1520m); and Chincoteague Island seep (CTS; ~1000m)). Mitochondrial COI (N = 162) and ND4 (N = 39) data suggest that Bathymodiolus childressi predominates at these sites, although single B. mauritanicus and B. heckerae individuals were detected. As previous work had suggested that methanotrophic and thiotrophic interactions can both occur at a site, and within an individual mussel, we investigated the symbiont communities in gill tissues of a subset of mussels from BCS and NCS. We constructed metabarcode libraries with four different primer sets spanning the 16S gene. A methanotrophic phylotype dominated all gill microbial samples from BCS, but sulfur-oxidizing Campylobacterota were represented by a notable minority of sequences from NCS. The methanotroph phylotype shared a clade with globally distributed Bathymodiolus spp. symbionts from methane seeps and hydrothermal vents. Two distinct Campylobacterota phylotypes were prevalent in NCS samples, one of which shares a clade with Campylobacterota associated with B. childressi from the Gulf of Mexico and the other with Campylobacterota associated with other deep-sea fauna. Variation in chemosynthetic symbiont communities among sites and individuals has important ecological and geochemical implications and suggests shifting reliance on methanotrophy. Continued characterization of symbionts from cold seeps will provide a greater understanding of the ecology of these unique environments as well and their geochemical footprint in elemental cycling and energy flux.

Incorporation of deep-sea and small-sized species provides new insights into gastropods phylogeny

The use of phylogeny with uneven or limited taxon sampling may bias our interpretation of organismal evolution, for instance, the origin(s) of the deep-sea animals. The Mollusca is the second most speciose phylum, in which the Gastropoda forms the largest group. However, the currently proposed hypotheses of gastropod phylogeny are mainly based on part of their taxonomic diversity, notably on the large-sized and shallow-water species. In this study, we aimed at correcting this bias by reconstructing the phylogeny with new mitogenomes of deep-sea gastropods including Anatoma sp., Bathysciadiidae sp., Bayerotrochus teramachii, Calliotropis micraulax, Coccocrater sp., Cocculina subcompressa, Lepetodrilus guaymasensis, Peltospira smaragdina, Perotrochus caledonicus, Pseudococculinidae sp., and Shinkailepas briandi. This dataset provided the first reports of the mitogenomes for the Cocculiniformia, three vetigastropod superfamilies: Pleurotomarioidea, Lepetelloidea, and Scissurelloidea, and the neritimorph family Phenacolepadidae. The addition of deep-sea representatives also allowed us to evaluate the evolution of habitat use in gastropods. Our results showed a strongly supported sister-group relationship between the deep-sea lineages Cocculiniformia and Neomphalina. Within the Vetigastropoda, the Pleurotomarioidea was revealed as the sister-group of the remaining vetigastropods. Although this clade was presently restricted to the deep sea, fossil records showed that it has only recently invaded this habitat, thus suggesting that shallow waters was the ancestral habitat for the Vetigastropoda. The deep-sea Lepetelloidea and Lepetodriloidea formed a well-supported clade, with the Scissurelloidea sister to it, suggesting an early transition from shallow water to deep sea in this lineage. In addition, the switch between different chemosynthetic habitats was also observed in deep-sea gastropod lineages, notably in Neomphalina and Lepetelloidea. In both cases, the biogenic substrates appeared as the putative ancestral habitat, confirming the previously proposed hypothesis of a wooden-step to deep-sea vents scenario of evolution of habitat use for these taxa.

Trophic structure and chemosynthesis contributions to heterotrophic fauna inhabiting an abyssal whale carcass

The trophic structure and role of chemosynthesis remain unexplored in deep-sea whale-fall communities in areas other than the California margin. This gap limits the understanding of these communities and their ecological relationships with other chemosynthetic ecosystems, such as vents and seeps. Here, we studied 3 different whale skeleton microhabitats with hypothesized high, intermediate and low reducing conditions as well as the sediments surrounding an abyssal whale fall (4204 m depth, SW Atlantic Ocean). We analyzed trophic structures (δ13C and δ15N) and the contribution of chemosynthetically derived carbon to heterotrophic species. The high and intermediate reducing microhabitats harbored food webs dominated by consumers of chemosynthetic production, similar to those of diffusive areas of hydrothermal vents and seeps. Both the low reducing microhabitat and the sediments harbored food webs with greater trophic complexity, dominated by higher consumers mainly relying on whale and/or photosynthesis-derived organic matter, a type of food web commonly reported in small whale, wood and kelp falls. The main whale-fall ecosystem engineer, the bone-eating worm Osedax, appeared to produce unique food web effects not observed in other chemosynthetic habitats. We conclude that whale falls provide the deep sea with a mosaic of microhabitats that supports assemblages with different chemosynthesis reliance levels and trophic structures, similar to those found at vents and seeps. Such a mosaic allows species-rich communities with numerous trophic levels to develop in a very small area of the food-limited deep sea.

Stylet jaws of Chrysopetalidae (Annelida)

ABSTRACTMicro-CT imaging elucidates jaw and pharynx structure in 14 nominal taxa belonging to Chrysopetalinae, Dysponetinae and Calamyzinae (Chrysopetalidae: Annelida). Systematic evaluation of chrysopetalid jaw form in each taxon is used to compare inter-generic relationships within and between each subfamily and with other polychaete families possessing lateral pairs of jaws. Jaw morphology proves diagnostic at all levels including agreement with current molecular phylogenetic analyses of the Chrysopetalidae. The greatest diversity of pharynx and jaw form, associated with sensory body characters, is found amongst taxa of the epibenthic Chrysopetalinae. It is hypothesized that the paired stylet jaws interlock to pierce prey tissue, and, in concert with a highly muscular pharynx, suck out prey fluids that pass down the internal groove of the stylets. Three generic groups are identified based on congruence of jaw form, and novel buccal structures are revealed in some taxa: a pharyngeal calcareous ‘ring’ and extensive pharyngeal glands. A continuum across free-living and facultative symbiont lifestyles is represented across all Chrysopetalinae. Dysponetinae comprises free-living, very small individuals that exhibit a meiofaunal lifestyle. All species possess one type of simple, tanned rod-like stylet jaws and certain simplified body structures. Calamyzinae species possess polyphyletic jaw forms and grades of radically simplified sensory morphologies. Free-living, bacteriovore calamyzins inhabit extreme chemosynthetic habitats and lack jaws, or possess modified jaws composed of an anterior platelet and posterior grooved jaw, present in the larvae and lost in the adult. New observations of an ectoparasitic Calamyzinae include details of a specialized mouth opening and stylet jaw present in a species that exhibits cryptic coloration, while grooved jaws are revealed for the first time in an obligate symbiont calamyzin. The grooved jaw form is considered a non-homoplasious synapomorphy that supports the monophyly of the family Chrysopetalidae.