The Mitochondrial Genomes of Siboglinum plumosum and Oligobrachia dogieli (Annelida: Siboglinidae) and Their Phylogenetic Analysis.

Frenulates are a group of sedentary Annelida within the family Siboglinidae that inhabit the ocean floor and present a unique challenge for comprehensive molecular and phylogenetic investigations. In this study, we focused on the frenulates, specifically assembling the mitochondrial genomes of Siboglinum plumosum and Oligobrachia dogieli. The phylogenetic reconstruction placed S. plumosum as a sister taxon to S. ekmani, and O. dogieli as a sister taxon to S. fiordicum, supporting the non-monophyletic nature of the genus Siboglinum. Overall, this study supports the phylogeny of the family Siboglinidae while highlighting the need for additional molecular data within frenulates.

Updated phylogeny of Vestimentifera (Siboglinidae, Polychaeta, Annelida) based on mitochondrial genomes, with a new species.

Siboglinid tubeworms are found at chemosynthetic environments worldwide and the Vestimentifera clade is particularly well known for their reliance on chemoautotrophic bacterial symbionts for nutrition. The mitochondrial genomes have been published for nine vestimentiferan species to date. This study provides new complete mitochondrial genomes for ten further Vestimentifera, including the first mitochondrial genomes sequenced for Alaysia spiralis, Arcovestia ivanovi, Lamellibrachia barhami, Lamellibrachia columna, Lamellibrachia donwalshi, and unnamed species of Alaysia and Oasisia. Phylogenetic analyses combining fifteen mitochondrial genes and the nuclear 18S rRNA gene recovered Lamellibrachia as sister to the remaining Vestimentifera and Riftia pachyptila as separate from the other vent-endemic taxa. Implications and auxiliary analyses regarding differing phylogenetic tree topologies, substitution saturation, ancestral state reconstruction, and divergence estimates are also discussed. Additionally, a new species of Alaysia is described from the Manus Basin.

Opportunistic consumption of marine pelagic, terrestrial, and chemosynthetic organic matter by macrofauna on the Arctic shelf: a stable isotope approach.

Macrofauna can contribute substantially to the organic matter cycling on the seafloor, yet the role of terrestrial and chemosynthetic organic matter in the diets of microphagous (deposit and suspension) feeders is poorly understood. In the present study, we used stable isotopes of carbon and nitrogen to test the hypothesis that the terrestrial organic matter supplied with river runoff and local chemosynthetic production at methane seeps might be important organic matter sources for macrofaunal consumers on the Laptev Sea shelf. We sampled locations from three habitats with the presumed differences in organic matter supply: "Delta" with terrestrial inputs from the Lena River, "Background" on the northern part of the shelf with pelagic production as the main organic matter source, and "Seep" in the areas with detected methane seepage, where chemosynthetic production might be available. Macrobenthic communities inhabiting each of the habitats were characterized by a distinct isotopic niche, mostly in terms of δ13C values, directly reflecting differences in the origin of organic matter supply, while δ15N values mostly reflected the feeding group (surface deposit/suspension feeders, subsurface deposit feeders, and carnivores). We conclude that both terrestrial and chemosynthetic organic matter sources might be substitutes for pelagic primary production in the benthic food webs on the largely oligotrophic Laptev Sea shelf. Furthermore, species-specific differences in the isotopic niches of species belonging to the same feeding group are discussed, as well as the isotopic niches of the symbiotrophic tubeworm Oligobrachia sp. and the rissoid gastropod Frigidoalvania sp., which are exclusively associated with methane seeps.

Finds of Siboglinids (Annelida, Siboglinidae) in the Estuaries of the Largest Arctic Rivers Are Associated with Permafrost Gas Hydrates.

Gutless marine worms of the family Siboglinidae have been found in the estuaries of the largest Arctic rivers Yenisei, Lena, and Mackenzie. Siboglinid metabolism is provided by symbiotic chemoautotrophic bacteria. Strong salinity stratification is characteristic of the estuaries of the largest Arctic rivers and ensures a high salinity at depths of 25-36 m, where siboglinids were found. High methane concentrations, which are necessary for siboglinid metabolism, result from dissociation of permafrost gas hydrates under the influence of river runoff in the conditions of Arctic warming.

Distribution of Siboglinids (Annelida, Siboglinidae) in the Laptev Sea and Adjacent Areas of the Arctic Basin.

Biodiversity in the Laptev Sea was assessed for gutless marine worms of the family Siboglinidae (Annelida), whose metabolism is provided by symbiotic bacteria that oxidize hydrogen sulfide and methane. Seven siboglinid species were found within the geographical boundaries of the Laptev Sea, and another species was found in an adjacent sector of the Arctic Basin. The largest number of finds and the greatest biological diversity of siboglinids were observed in the eastern part of the Laptev Sea in a field of numerous methane flares. One find was made in the estuary area of the Lena River at a depth of 25 m. A possible association of siboglinids with methane seepage areas is discussed.

The Finding of Pogonophorans (Annelida, Siboglinidae) in the St. Anna Trough (Kara Sea) in an Area of Gas Hydrate Dissociation.

Representatives of pogonophorans (Annelida, Siboglinidae), whose vital activity is provided by symbiotic chemoautotrophic bacteria that oxidize methane and hydrogen sulfide, were found in the St. Anna Trough at depths of 539 and 437 m. The finding of pogonophorans suggests high concentrations of methane, which might result from dissociation of bottom gas hydrates under the influence of the influx of warm Atlantic water into the Kara Sea along the St. Anna Trough.

Apoptotic Processes Precede Infection with Symbionts in a Pogonophoran Lavrae (Siboglinidae, Annelida).

The fine structure of the body wall and gut was for the first time studied in the competent larvae of the frenulate pogonophoran Siboglinum fiordicum. Mass apoptosis of cell nuclei was observed in the dermo-muscular body wall and coelomic epithelium. Apoptotic nuclei were found in both cell cytoplasm and outside of the larval body. In the latter case, each nucleus was surrounded by the plasmalemma, and the entire cluster was covered with the cuticle. Cells of the larval gut retained the usual structure with the cytoplasm filled with numerous yolky granules and the nucleus displaying usual morphology. Similar apoptotic processes have been described in vestimentiferans and found to be initiated by penetration of symbiotic bacteria through the integument into the dorsal mesentery. The process of apoptotic rearrangement of body wall cells and the formation of unique symbiosis with bacteria were assumed to be time-spaced in S. fiordicum, occurring sequentially rather than simultaneously, unlike in vestimentiferans.

First Experience of Keeping Pogonophorans (Annelida: Siboglinidae) in Laboratory Conditions.

The article describes the parameters of maintaining the gutless symbiotrophic annelid Siboglinum fiordicum in laboratory conditions outside the marine environment for 64 days.

New Data on Distribution of Nereilinum murmanicum (Annelida, Siboglinidae) in the Barents Sea.

The article presents a report on the findings of representatives of frenulate pogonophorans Nereilinum murmanicum in the northern and central parts of the Barents Sea, which significantly expands the range of this species and provides guidance on its distribution in this basin. Here we present the coordinates of new finds with an indication of the depth. Find points were associated with data on known and potential hydrocarbon deposits.

Structure and Origin of the Vestimentiferan Trophosome (Annelida, Siboglinidae).

The anatomical and histological structure of the trophosome of the giant vestimentiferan Riftiapachyptila has been studied. The trophosome consists of longitudinally oriented cords. The cords of the trophosome intertwine, form diverticula and anastomose with each other. Each cord has an axial blood vessel inside, which is connected to afferent vessels on the surface of the cord by radial capillaries. Based on the data on the structure and development of the trophosome, it is suggested that the evolutionary precursor of the trophosome was a blood network connecting the ventral and dorsal vessels. The cells of the coelomic lining on the surface of the vessels grew and gave rise to the parenchymal tissue of the trophosome. At the same time, the trophosome developed from two sources, namely: due to the coelomic lining on the surface of the vessels of the intestinal plexus and due to the coelomic lining on the surface of the vessels of the circulatory plexus of the body wall.

Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000.

BACKGROUND: The nervous system of siboglinids has been studied mainly in Osedax and some Vestimentifera, while data in Frenulata - one of the four pogonophoran main branches - is still fragmentary. In most of the studies, the focus is almost always on the central nervous system, while the peripheral nervous system has traditionally received little attention. In contrast to other annelids, the structure and diversity of sensory structures in siboglinids are still quite undescribed. Meanwhile, the peripheral nervous system, as well as sensory elements, are extremely evolutionarily labile, and information about their organization is of high importance to understand lifestyles and behavior as well as main trends that lead siboglinids to their peculiar organization. RESULTS: The structure of the peripheric nervous system, sensory elements, and neuromuscular relationships of Oligobrachia haakonmosbiensis were studied using both scanning electron and confocal laser microscopy. A significant number of monociliary sensory cells, as well as sensory complexes located diffusely in the epithelium of the whole body were revealed. The latter include the cephalic tentacles, sensory cells accumulations along the dorsal furrow and ciliary band, areas of the openings of the tubiparous glands, and papillae. The oval ciliary spot located on the cephalic lobe at the base of the tentacles can also be regarded as a sensory organ. Most of the detected sensory cells show immunoreactivity to substance P and/or acetylated α-tubulin. FMRFamide- and serotonin-like immunoreactivity are manifested by neurons that mainly innervate tentacles, muscles, body wall epithelium, skin glands, tubiparous glands, and papillae. In the larva of O. haakonmosbiensis, monociliary sensory elements were revealed in the region of the apical organ, along the body, and on the pygidium. CONCLUSIONS: The diversity of sensory structures in O. haakonmosbiensis comprises epidermal solitary sensory cells, sensory spots around tubiparous glands openings, and putative sensory organs such as cephalic tentacles, an oval ciliary spot on the cephalic lobe, the dorsal furrow, and papillae. Sensory structures associated with papillae and tubiparous glands play presumable mechanosensory functions and are associated with regulation of tube building as well as anchorage of the worm inside the tube. Sensory structures of the dorsal furrow are presumably engaged in the regulation of reproductive behavior. An overall low level of morphological differentiation of O. haakonmosbiensis peripheral nervous system is not typical even for annelids with the intraepithelial nervous system. This can be considered as a plesiomorphic feature of its peripheral plexus's organization, or as evidence for the neotenic origin of Siboglinidae.

The First Discovery of Pogonophora (Annelida, Siboglinidae) in the East Siberian Sea Coincides with the Areas of Methane Seeps.

Pogonophora or siboglinid tubeworms (Annelida, Siboglinidae) have been found in the East Siberian Sea for the first time. On the basis of the results of molecular phylogenetic analysis, the found specimens are presumably assigned to the genus Oligobrachia. The stations where the siboglinid tubeworms have been found are located in the area of methane seeps. This confirms the previously stated hypothesis about relationship of siboglinid tubeworm distribution with the areas of underwater methane seeps.

Obturacula of Vestimentifera (Annelida, Siboglinidae) Are Homological to the Dorsal Lips of the Polychaete of the Family Sabellidae.

We have conducted comparative analysis of the structure of the dorsal lips of the polychaete Eudistylia polymorpha from the family Sabellidae and the obturacula of Oasisia alvinae (Vestimentifera). It has been concluded that the obturacula of Vestimentifera are homologs of the dorsal lips of Polychaete from the family Sabellidae. It has been suggested that the head lobe of siboglinids of the subfamily Frenulata is homologous to the fused obturacula of Vestimentifera.

First Discovery of Pogonophora (Annelida, Siboglinidae) in the Kara Sea Coincide with the Area of High Methane Concentration.

Here we report the first finding of a frenulate pogonophoran (Annelida, Siboglinidae) in the southern part of the Kara Sea. This finding was made in the Yenisei Gulf in the region of the highest methane concentrations, resulting from the degradation of permafrost under the influence of river flow. It has been suggested that pogonophorans are indicators of hydrocarbon manifestations of various genesis.

Siboglinidae Tubes as an Additional Niche for Microbial Communities in the Gulf of Cádiz-A Microscopical Appraisal.

Siboglinids were sampled from four mud volcanoes in the Gulf of Cádiz (El Cid MV, Bonjardim MV, Al Gacel MV, and Anastasya MV). These invertebrates are characteristic to cold seeps and are known to host chemosynthetic endosymbionts in a dedicated trophosome organ. However, little is known about their tube as a potential niche for other microorganisms. Analyses by scanning and transmission electron microscopy showed dense biofilms on the tube in Al Gacel MV and Anastasya MV specimens by prokaryotic cells. Methanotrophic bacteria were the most abundant forming these biofilms as further supported by 16S rRNA sequence analysis. Furthermore, elemental analyses with electron microscopy and energy-dispersive X-ray spectroscopy point to the mineralization and silicification of the tube, most likely induced by the microbial metabolisms. Bacterial and archaeal 16S rRNA sequence libraries revealed abundant microorganisms related to these siboglinid specimens and certain variations in microbial communities among samples. Thus, the tube remarkably increases the microbial biomass related to the worms and provides an additional microbial niche in deep-sea ecosystems.

An inordinate fondness for Osedax (Siboglinidae: Annelida): Fourteen new species of bone worms from California.

We incorporate DNA sequences from a comprehensive sampling of taxa to provide an updated phylogeny of Osedax and discuss the remarkable diversity of this clade of siboglinids. We formally describe 14 new species of Osedax from Monterey Bay, California, USA, raising the total number of properly named Osedax species to 25. These new species had formerly been recognized by informal names in various publications, and on GenBank. The descriptions document the occurrence of dwarf males in five of the new species. The distribution for the 19 species of Osedax known to occur in Monterey Bay across depths from 385 to 2898 meters and various bone substrates is documented. The exploitation of extant bird and marine turtle bones by Osedax is reported for the first time.

Extreme longevity in a deep-sea vestimentiferan tubeworm and its implications for the evolution of life history strategies.

The deep sea is home to many species that have longer life spans than their shallow-water counterparts. This trend is primarily related to the decline in metabolic rates with temperature as depth increases. However, at bathyal depths, the cold-seep vestimentiferan tubeworm species Lamellibrachia luymesi and Seepiophila jonesi reach extremely old ages beyond what is predicted by the simple scaling of life span with body size and temperature. Here, we use individual-based models based on in situ growth rates to show that another species of cold-seep tubeworm found in the Gulf of Mexico, Escarpia laminata, also has an extraordinarily long life span, regularly achieving ages of 100-200 years with some individuals older than 300 years. The distribution of results from individual simulations as well as whole population simulations involving mortality and recruitment rates support these age estimates. The low 0.67% mortality rate measurements from collected populations of E. laminata are similar to mortality rates in L. luymesi and S. jonesi and play a role in evolution of the long life span of cold-seep tubeworms. These results support longevity theory, which states that in the absence of extrinsic mortality threats, natural selection will select for individuals that senesce slower and reproduce continually into their old age.

Complete mitochondrial genome of the hydrothermal vent tubeworm, Ridgeia piscesae (Polychaeta, Siboglinidae).

The complete mitochondrial genome of Ridgeia piscesae (Polychaeta, Siboglinidae), one of the dominant taxa in deep-sea hydrothermal vents, is reported here for the first time. The R. piscesae mitogenome is 15,002 bp in total length and includes 13 protein-coding gene sequences, small and large rRNA sequences and 22 tRNA sequences. All genes are encoded on the heavy strand. The mitochondrial genomes of R. piscesae and other six polychaete species have a conserved gene order.

Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls.

We report fossil traces of Osedax, a genus of siboglinid annelids that consume the skeletons of sunken vertebrates on the ocean floor, from early-Late Cretaceous (approx. 100 Myr) plesiosaur and sea turtle bones. Although plesiosaurs went extinct at the end-Cretaceous mass extinction (66 Myr), chelonioids survived the event and diversified, and thus provided sustenance for Osedax in the 20 Myr gap preceding the radiation of cetaceans, their main modern food source. This finding shows that marine reptile carcasses, before whales, played a key role in the evolution and dispersal of Osedax and confirms that its generalist ability of colonizing different vertebrate substrates, like fishes and marine birds, besides whale bones, is an ancestral trait. A Cretaceous age for unequivocal Osedax trace fossils also dates back to the Mesozoic the origin of the entire siboglinid family, which includes chemosynthetic tubeworms living at hydrothermal vents and seeps, contrary to phylogenetic estimations of a Late Mesozoic-Cenozoic origin (approx. 50-100 Myr).

Segment regeneration in the vestimentiferan tubeworm, Lamellibrachia satsuma.

The ability to regenerate missing body parts varies among species. To elucidate the evolution of regenerative capability, an understanding of the regeneration mechanisms of diverse organisms is required. We focus on vestimentiferan tubeworms, which have a body plan that is unique among annelids. We found that the vestimentiferan Lamellibrachia satsuma is able to regenerate its posterior body parts, but not its anterior body parts. Based on observations of live specimens, we defined five stages in the process of posterior regeneration. The morphogenesis was observed in detail by a series of sections and scanning electron microscopy. The most posterior domain of the opisthosome differentiated from the blastema, while the anterior domain of the opisthosome regenerated from the remaining trunk region. We also examined the expression pattern of the engrailed gene during regeneration, and found that engrailed was expressed in the mesodermal cells of each segment.