Vision in hydrothermal vent shrimp

Bresiliid shrimp from hydrothermal vents on the Mid-Atlantic Ridge have non-imaging eyes adapted for photodetection in light environments of very low intensity. Comparison of retinal structures between both vent shrimp and surface-dwelling shrimp with imaging eyes, and between juvenile and adult vent shrimp, suggests that vent shrimp have evolved from ancestors that lived in a light environment with bright cyclic lighting. Whether the vent shrimp live in swarms and have large dorsal eyes or live in sparse groupings and have large anterior eyes, the basic retinal adaptations are the same across species. Retinal adaptations in adult vent shrimp include the loss of dioptrics, enlargement of both the rhabdomeral segment of the photoreceptors and the light-sensitive rhabdomere therein, attenuation of the arhabdomeral segment of the photoreceptors, reduction of black screening pigment, development of a white diffusing layer behind the photoreceptors, and the loss of rhabdom turnover.     

A hydrothermal seep on the Costa Rica margin: middle ground in a continuum of reducing ecosystems

Upon their initial discovery, hydrothermal vents and methane seeps were considered to be related but distinct ecosystems, with different distributions, geomorphology, temperatures, geochemical properties and mostly different species. However, subsequently discovered vents and seep systems have blurred this distinction. Here, we report on a composite, hydrothermal seep ecosystem at a subducting seamount on the convergent Costa Rica margin that represents an intermediate between vent and seep ecosystems. Diffuse flow of shimmering, warm fluids with high methane concentrations supports a mixture of microbes, animal species, assemblages and trophic pathways with vent and seep affinities. Their coexistence reinforces the continuity of reducing environments and exemplifies a setting conducive to interactive evolution of vent and seep biota.     

The contrasted evolutionary fates of deep‐sea chemosynthetic mussels (Bivalvia,Bathymodiolinae)

Bathymodiolinae are giant mussels that were discovered at hydrothermal vents and harboring chemosynthetic symbionts. Due to their close phylogenetic relationship with seep species and tiny mussels from organic substrates, it was hypothesized that they gradually evolved from shallow to deeper environments, and specialized in decaying organic remains, then in seeps, and finally colonized deep‐sea vents. Here, we present a multigene phylogeny that reveals that most of the genera are polyphyletic and/or paraphyletic. The robustness of the phylogeny allows us to revise the genus‐level classification. Organic remains are robustly supported as the ancestral habitat for Bathymodiolinae. However, rather than a single step toward colonization of vents and seeps, recurrent habitat shifts from organic substrates to vents and seeps occurred during evolution, and never the reverse. This new phylogenetic framework challenges the gradualist scenarios “from shallow to deep.” Mussels from organic remains tolerate a large range of ecological conditions and display a spectacular species diversity contrary to vent mussels, although such habitats are yet underexplored compared to vents and seeps. Overall, our data suggest that for deep‐sea mussels, the high specialization to vent habitats provides ecological success in this harsh habitat but also brings the lineage to a kind of evolutionary dead end.     

Physiological Ecology of Sulfide Metabolism in Hydrothermal Vent and Cold Seep Vesicomyid Clams and Vestimentiferan Tube Worms

SYNOPSIS. The primary ecosystem-structuring organisms at manyhydrothermal vents and cold seeps are phylogenetically relatedand quite similar physiologically and anatomically. Vestimentiferantube worms and Vesicomyid clams in particular all rely on chemoautotrophicsulfur-oxidizing symbionts and have blood which binds sulfidewith high affinity and capacity. However, there are significantdifferences between cold seep and hydrothermal vent environments,including large differences in flow rate of the emitted fluidand the chemistry of that fluid. Here we review extant dataon the hydrothermal vent species, present new data on the physiologicallyrelevant chemical microhabitat of cold seep vestimentiferansand vesicomyids, and compare the physiological ecology of theseep species to their hydrothermal vent relatives     

Expansion of the geographic distribution of a novel lineage of epsilon-Proteobacteria to a hydrothermal vent site on the Southern East Pacific Rise

The diversity associated with a microbial mat sample collected from a deep-sea hydrothermal vent on the Southern East Pacific Rise was determined using a molecular phylogenetic approach based on the comparison of sequences from the small subunit ribosomal RNA gene (16S rDNA). The DNA was extracted from the sample and the 16S rDNA was amplified by PCR. Sixteen different phylotypes were identified by restriction fragment length polymorphism analysis; four phylotypes were later identified as putative chimeras. Analysis of the 16S rDNA sequences placed all the phylotypes within the Proteobacteria. The majority of the sequences (98%) were most closely related to a new clade of epsilon-Proteobacteria that were initially identified from an in situ growth chamber deployed on a deep-sea hydrothermal vent on the Mid-Atlantic Ridge in 1995. The similarity between phylotypes identified from Atlantic and Pacific deep-sea hydrothermal vent sites indicates that this new clade of Proteobacteria may be endemic to and widely distributed among deep-sea hydrothermal vents.     

The discovery of new deep-sea hydrothermal vent communities in the southern ocean and implications for biogeography

Since the first discovery of deep-sea hydrothermal vents along the Galápagos Rift in 1977, numerous vent sites and endemic faunal assemblages have been found along mid-ocean ridges and back-arc basins at low to mid latitudes. These discoveries have suggested the existence of separate biogeographic provinces in the Atlantic and the North West Pacific, the existence of a province including the South West Pacific and Indian Ocean, and a separation of the North East Pacific, North East Pacific Rise, and South East Pacific Rise. The Southern Ocean is known to be a region of high deep-sea species diversity and centre of origin for the global deep-sea fauna. It has also been proposed as a gateway connecting hydrothermal vents in different oceans but is little explored because of extreme conditions. Since 2009 we have explored two segments of the East Scotia Ridge (ESR) in the Southern Ocean using a remotely operated vehicle. In each segment we located deep-sea hydrothermal vents hosting high-temperature black smokers up to 382.8°C and diffuse venting. The chemosynthetic ecosystems hosted by these vents are dominated by a new yeti crab (Kiwa n. sp.), stalked barnacles, limpets, peltospiroid gastropods, anemones, and a predatory sea star. Taxa abundant in vent ecosystems in other oceans, including polychaete worms (Siboglinidae), bathymodiolid mussels, and alvinocaridid shrimps, are absent from the ESR vents. These groups, except the Siboglinidae, possess planktotrophic larvae, rare in Antarctic marine invertebrates, suggesting that the environmental conditions of the Southern Ocean may act as a dispersal filter for vent taxa. Evidence from the distinctive fauna, the unique community structure, and multivariate analyses suggest that the Antarctic vent ecosystems represent a new vent biogeographic province. However, multivariate analyses of species present at the ESR and at other deep-sea hydrothermal vents globally indicate that vent biogeography is more complex than previously recognised.     

High contents of hypotaurine and thiotaurine in hydrothermal-vent gastropods without thiotrophic endosymbionts

Invertebrates at hydrothermal vents and cold seeps must cope with high levels of toxic H2S. In addition, these and all marine invertebrates must balance internal osmotic pressure with that of the ocean. Cells usually do so with organic osmolytes, primarily free amino acids (e.g., taurine, glycine) and methylamines (e.g., betaine). At vents and seeps, clams, mussels, and vestimentiferans with thiotrophic endosymbionts have high levels of hypotaurine and thiotaurine (a product of hypotaurine and HS-). These serve as osmolytes but their primary function may be to transport and/or detoxify sulfide; indeed, thiotaurine has been proposed to be a marker of thiotrophic symbiosis. To test this, we analyzed Depressigyra globulus snails and Lepetodrilus fucensis limpets from Juan de Fuca Ridge vents (1,530 m). Neither has endosymbionts, though the latter has thiotrophic ectosymbionts. Some specimens were rapidly frozen, while other live ones were kept in laboratory chambers, some with and others without sulfide. Non-vent gastropods from a variety of depths (2-3,000 m) were also collected. Tissues were analyzed for major osmolytes and taurine derivatives. The dominant osmolytes of non-vent snails were betaine in all species, and either taurine in shallow-living species or scyllo-inositol, glycerophosphorylcholine, and other amino acids in deep-sea species. In contrast, the dominant osmolytes were hypotaurine and betaine in D. globulus, and hypotaurine in L. fucensis. Both species had thiotaurine (as well as hypotaurine) at levels much greater than previously reported for vent and seep animals without endosymbionts. The ratio of thio- to thio- plus hypotaurine, a possible indicator of sulfide exposure, decreased in both species when kept in laboratory chambers with low or no sulfide, but stayed at high levels in snails kept with 3-5 mM sulfide. Thus, in some vent animals without endosymbionts, sulfide may be detoxified via conversion of hypotaurine to thiotaurine. The latter may be a marker of high sulfide exposure but not of thiotrophic endosymbionts.     

Draft genome sequence of Caminibacter mediatlanticus strain TB-2, an epsilonproteobacterium isolated from a deep-sea hydrothermal vent

Caminibacter mediatlanticus strain TB-2(T) [1], is a thermophilic, anaerobic, chemolithoautotrophic bacterium, isolated from the walls of an active deep-sea hydrothermal vent chimney on the Mid-Atlantic Ridge and the type strain of the species. C. mediatlanticus is a Gram-negative member of the Epsilonproteobacteria (order Nautiliales) that grows chemolithoautotrophically with H(2) as the energy source and CO(2) as the carbon source. Nitrate or sulfur is used as the terminal electron acceptor, with resulting production of ammonium and hydrogen sulfide, respectively. In view of the widespread distribution, importance and physiological characteristics of thermophilic Epsilonproteobacteria in deep-sea geothermal environments, it is likely that these organisms provide a relevant contribution to both primary productivity and the biogeochemical cycling of carbon, nitrogen and sulfur at hydrothermal vents. Here we report the main features of the genome of C. mediatlanticus strain TB-2(T).     

Off-axis symbiosis found: Characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents

Organisms at hydrothermal vents inhabit discontinuous chemical 'islands' along mid-ocean ridges, a scenario that may promote genetic divergence among populations. The 2003 discovery of mussels at the Lost City Hydrothermal Field provided a means of evaluating factors that govern the biogeography of symbiotic bacteria in the deep sea. The unusual chemical composition of vent fluids, the remote location, and paucity of characteristic vent macrofauna at the site, raised the question of whether microbial symbioses existed at the extraordinary Lost City. If so, how did symbiotic bacteria therein relate to those hosted by invertebrates at the closest known hydrothermal vents along the Mid-Atlantic Ridge (MAR)? To answer these questions, we performed microscopic and molecular analyses on the bacteria found within the gill tissue of Bathymodiolus mussels (Mytilidae, Bathymodiolinae) that were discovered at the Lost City. Here we show that Lost City mussels harbour chemoautotrophic and methanotrophic endosymbionts simultaneously. Furthermore, populations of the chemoautotrophic symbionts from the Lost City and two sites along the MAR are genetically distinct from each other, which suggests spatial isolation of bacteria in the deep sea. These findings provide new insights into the processes that drive diversification of bacteria and evolution of symbioses at hydrothermal vents.     

Diversity in mussel beds at deep-sea hydrothermal vents and cold seeps

Remarkably little is known about fundamental distinctions (or similarities) between the faunas of deep‐sea hydrothermal vents and seeps. Low species richness at vents has been attributed to the transient nature of vent habitats and to toxic effects of hydrogen sulphide and heavy metals in vent effluents. Seeps are arguably more stable and more chemically benign than vents. They have also been regarded as more diverse, but until now there has not been a rigorous test of this hypothesis. We evaluated diversity indices for invertebrates associated with mussel beds at six vents and two seeps and found that invertebrate diversity was significantly higher at seeps than vents, although some vent mussel beds supported nearly the same diversity as seep mussel beds. Lower diversity at vents may be a consequence of a greater physiological barrier to invasion at vents than at seeps. Diversity was lowest where spacing between vents was greatest, suggesting that risks of extinction as a result of dispersal‐related processes may contribute to the pattern of diversity observed at vents.     

Occurrence and recent long-distance dispersal of deep-sea hydrothermal vent shrimps

Deep-sea hydrothermal vents and methane seeps are extreme environments that have a high concentration of hydrogen sulphide. However, abundant unique invertebrates including shrimps of the family Bresiliidae have been found in such environments. The bresiliid shrimps are believed to have radiated in the Miocene (less than 20 Myr); however, the period when and the mechanisms by which they dispersed across the hydrothermal vents and cold seeps in oceans worldwide have not been clarified. In the present study, we collected the deep-sea blind shrimp Alvinocaris longirostris from the hydrothermal vent site in the Okinawa Trough and carried out the first investigation of the 18S rRNA gene of a bresiliid shrimp. The phylogenetic analysis revealed that the bresiliid shrimp is situated at an intermediate lineage within the infraorder Caridea and shows monophyly with palaemonid shrimps, which live in shallow sea and freshwater. Furthermore, the mitochondrial cytochrome oxidase I (COI) gene sequences were analysed to determine the phylogenetic relationship with known bresiliid shrimps. A. longirostris of the Okinawa Trough had two haplotypes of the COI gene, one of which was identical to the Alvinocaris sp. of the cold seeps in Sagami Bay. These results indicate that a long-distance dispersal of A. longirostris occurred possibly within the last 100,000 years.     

Ecology and Biogeography of Free-Living Nematodes Associated with Chemosynthetic Environments in the Deep Sea: A Review

Background

Here, insight is provided into the present knowledge on free-living nematodes associated with chemosynthetic environments in the deep sea. It was investigated if the same trends of high standing stock, low diversity, and the dominance of a specialized fauna, as observed for macro-invertebrates, are also present in the nematodes in both vents and seeps.

Methodology

This review is based on existing literature, in combination with integrated analysis of datasets, obtained through the Census of Marine Life program on Biogeography of Deep-Water Chemosynthetic Ecosystems (ChEss).

Findings

Nematodes are often thriving in the sulphidic sediments of deep cold seeps, with standing stock values ocassionaly exceeding largely the numbers at background sites. Vents seem not characterized by elevated densities. Both chemosynthetic driven ecosystems are showing low nematode diversity, and high dominance of single species. Genera richness seems inversely correlated to vent and seep fluid emissions, associated with distinct habitat types. Deep-sea cold seeps and hydrothermal vents are, however, highly dissimilar in terms of community composition and dominant taxa. There is no unique affinity of particular nematode taxa with seeps or vents.

Conclusions

It seems that shallow water relatives, rather than typical deep-sea taxa, have successfully colonized the reduced sediments of seeps at large water depth. For vents, the taxonomic similarity with adjacent regular sediments is much higher, supporting rather the importance of local adaptation, than that of long distance distribution. Likely the ephemeral nature of vents, its long distance offshore and the absence of pelagic transport mechanisms, have prevented so far the establishment of a successful and typical vent nematode fauna. Some future perspectives in meiofauna research are provided in order to get a more integrated picture of vent and seep biological processes, including all components of the marine ecosystem.     

Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields

The shrimp Rimicaris exoculata from hydrothermal vents on the Mid-Atlantic Ridge (MAR) harbours bacterial epibionts on specialized appendages and the inner surfaces of its gill chamber. Using comparative 16S rRNA sequence analysis and fluorescence in situ hybridization (FISH), we examined the R. exoculata epibiosis from four vents sites along the known distribution range of the shrimp on the MAR. Our results show that R. exoculata lives in symbiosis with two types of filamentous epibionts. One belongs to the Epsilonproteobacteria, and was previously identified as the dominant symbiont of R. exoculata. The second is a novel gammaproteobacterial symbiont that belongs to a clade consisting exclusively of sequences from epibiotic bacteria of hydrothermal vent animals, with the filamentous sulfur oxidizer Leucothrix mucor as the closest free-living relative. Both the epsilon- and the gammaproteobacterial symbionts dominated the R. exoculata epibiosis at all four MAR vent sites despite striking differences between vent fluid chemistry and distances between sites of up to 8500 km, indicating that the symbiosis is highly stable and specific. Phylogenetic analyses of two mitochondrial host genes showed little to no differences between hosts from the four vent sites. In contrast, there was significant spatial structuring of both the gamma- and the epsilonproteobacterial symbiont populations based on their 16S rRNA gene sequences that was correlated with geographic distance along the MAR. We hypothesize that biogeography and host-symbiont selectivity play a role in structuring the epibiosis of R. exoculata.     

Hidden Historical Habitat-Linked Population Divergence and Contemporary Gene Flow of a Deep-Sea Patellogastropod Limpet

Hydrothermal vents and hydrocarbon seeps in the deep ocean are rare oases fueled by chemosynthesis. Biological communities inhabiting these ecosystems are often distributed in widely separated habitats, raising intriguing questions on how these organisms achieve connectivity and whether habitat types facilitate intraspecific divergence. The deep-sea patellogastropod limpet Bathyacmaea nipponica that colonizes both vents and seeps across ∼2,400 km in the Northwest Pacific is a feasible model to answer these questions. We analyzed 123 individuals from four vents and three seeps using a comprehensive method incorporating population genomics and physical ocean modeling. Genome survey sequencing and genotyping-by-sequencing resulted in 9,838 single-nucleotide polymorphisms for population genomic analyses. Genetic divergence and demographic analyses revealed four habitat-linked (i.e., three seep and one vent) genetic groups, with the vent genetic group established via the opportunistic invasion of a few limpet larvae from a nearby seep genetic group. TreeMix analysis uncovered three historical seep-to-vent migration events. ADMIXTURE and divMigrate analyses elucidated weak contemporary gene flow from a seep genetic group to the vent genetic group. Physical ocean modeling underlined the potential roles of seafloor topography and ocean currents in shaping the genetic connectivity, contemporary migration, and local hybridization of these deep-sea limpets. Our study highlighted the power of integrating genomic and oceanographic approaches in deciphering the demography and diversification of deep-sea organisms. Given the increasing anthropogenic activities (e.g., mining and gas hydrate extraction) affecting the deep ocean, our results have implications for the conservation of deep-sea biodiversity and establishment of marine protected areas.     

Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels

Many parasitic bacteria live in the cytoplasm of multicellular animals, but only a few are known to regularly invade their nuclei. In this study, we describe the novel bacterial parasite “Candidatus Endonucleobacter bathymodioli” that invades the nuclei of deep‐sea bathymodiolin mussels from hydrothermal vents and cold seeps. Bathymodiolin mussels are well known for their symbiotic associations with sulfur‐ and methane‐oxidizing bacteria. In contrast, the parasitic bacteria of vent and seep animals have received little attention despite their potential importance for deep‐sea ecosystems. We first discovered the intranuclear parasite “Ca. E. bathymodioli” in Bathymodiolus puteoserpentis from the Logatchev hydrothermal vent field on the Mid‐Atlantic Ridge. Using primers and probes specific to “Ca. E. bathymodioli” we found this intranuclear parasite in at least six other bathymodiolin species from vents and seeps around the world. Fluorescence in situ hybridization and transmission electron microscopy analyses of the developmental cycle of “Ca. E. bathymodioli” showed that the infection of a nucleus begins with a single rod‐shaped bacterium which grows to an unseptated filament of up to 20 μm length and then divides repeatedly until the nucleus is filled with up to 80 000 bacteria. The greatly swollen nucleus destroys its host cell and the bacteria are released after the nuclear membrane bursts. Intriguingly, the only nuclei that were never infected by “Ca. E. bathymodioli” were those of the gill bacteriocytes. These cells contain the symbiotic sulfur‐ and methane‐oxidizing bacteria, suggesting that the mussel symbionts can protect their host nuclei against the parasite. Phylogenetic analyses showed that the “Ca. E. bathymodioli” belongs to a monophyletic clade of Gammaproteobacteria associated with marine metazoans as diverse as sponges, corals, bivalves, gastropods, echinoderms, ascidians and fish. We hypothesize that many of the sequences from this clade originated from intranuclear bacteria, and that these are widespread in marine invertebrates.     

Molecular and functional adaptations in deep-sea hemoglobins

The past 20 years have witnessed the publication of numerous studies on hemoglobins (Hbs) from deep-sea animals. Most of the animals studied were collected at deep-sea hydrothermal vents and cold seeps, both being environments where the physical-chemical conditions may be severely challenging for metazoans. These environments may be characterized by deep, chronic hypoxia and high concentrations of toxic compounds such as sulfide and heavy metals. Many species from these environments express Hbs, even though they belong to taxa that otherwise were characterised by the absence of respiratory pigments. Hbs from vent and seep invertebrates commonly exhibit high affinities for oxygen when compared to related species from normoxic, shallow-water environments, and marked pH-dependence. These high affinities permit uptake of oxygen from hypoxic waters and the strong Bohr effects favor its release in the metabolizing acidic organs.     

Characterization of Bacterial Communities in Deep-Sea Hydrothermal Vents from Three Oceanic Regions

Deep-sea hydrothermal vents are considered to be one of the most spectacular ecosystems on Earth. Microorganisms form the basis of the food chain in vents controlling the vent communities. However, the diversity of bacterial communities in deep-sea hydrothermal vents from different oceans remains largely unknown. In this study, the pyrosequencing of 16S rRNA gene was used to characterize the bacterial communities of the venting sulfide, seawater, and tubeworm trophosome from East Pacific Rise, South Atlantic Ridge, and Southwest Indian Ridge, respectively. A total of 23,767 operational taxonomic units (OTUs) were assigned into 42 different phyla. Although Proteobacteria, Actinobacteria, and Bacteroidetes were the predominant phyla in all vents, differences of bacterial diversity were observed among different vents from three oceanic regions. The sulfides of East Pacific Rise possessed the most diverse bacterial communities. The bacterial diversities of venting seawater were much lower than those of vent sulfides. The symbiotic bacteria of tubeworm Ridgeia piscesae were included in the bacterial community of vent sulfides, suggesting their significant ecological functions as the primary producers in the deep-sea hydrothermal vent ecosystems. Therefore, our study presented a comprehensive view of bacterial communities in deep-sea hydrothermal vents from different oceans.     

Microbial Iron Mats at the Mid-Atlantic Ridge and Evidence that Zetaproteobacteria May Be Restricted to Iron-Oxidizing Marine Systems

Chemolithoautotrophic iron-oxidizing bacteria play an essential role in the global iron cycle. Thus far, the majority of marine iron-oxidizing bacteria have been identified as Zetaproteobacteria, a novel class within the phylum Proteobacteria. Marine iron-oxidizing microbial communities have been found associated with volcanically active seamounts, crustal spreading centers, and coastal waters. However, little is known about the presence and diversity of iron-oxidizing communities at hydrothermal systems along the slow crustal spreading center of the Mid-Atlantic Ridge. From October to November 2012, samples were collected from rust-colored mats at three well-known hydrothermal vent systems on the Mid-Atlantic Ridge (Rainbow, Trans-Atlantic Geotraverse, and Snake Pit) using the ROV Jason II. The goal of these efforts was to determine if iron-oxidizing Zetaproteobacteria were present at sites proximal to black smoker vent fields. Small, diffuse flow venting areas with high iron(II) concentrations and rust-colored microbial mats were observed at all three sites proximal to black smoker chimneys. A novel, syringe-based precision sampler was used to collect discrete microbial iron mat samples at the three sites. The presence of Zetaproteobacteria was confirmed using a combination of 16S rRNA pyrosequencing and single-cell sorting, while light micros-copy revealed a variety of iron-oxyhydroxide structures, indicating that active iron-oxidizing communities exist along the Mid-Atlantic Ridge. Sequencing analysis suggests that these iron mats contain cosmopolitan representatives of Zetaproteobacteria, but also exhibit diversity that may be uncommon at other iron-rich marine sites studied to date. A meta-analysis of publically available data encompassing a variety of aquatic habitats indicates that Zetaproteobacteria are rare if an iron source is not readily available. This work adds to the growing understanding of Zetaproteobacteria ecology and suggests that this organism is likely locally restricted to iron-rich marine environments but may exhibit wide-scale geographic distribution, further underscoring the importance of Zetaproteobacteria in global iron cycling.