Neural reconstruction of bone-eating <i>Osedax</i> spp. (Annelida) and evolution of the siboglinid nervous system

BACKGROUND: Bone-devouring Osedax worms were described over a decade ago from deep-sea whale falls. The gutless females (and in one species also the males) have a unique root system that penetrates the bone and nourishes them via endosymbiotic bacteria. Emerging from the bone is a cylindrical trunk, which is enclosed in a transparent tube, that generally gives rise to a plume of four palps (or tentacles). In most Osedax species, dwarf males gather in harems along the female’s trunk and the nervous system of these microscopic forms has been described in detail. Here, the nervous system of bone-eating Osedax forms are described for the first time, allowing for hypotheses on how the abberant ventral brain and nervous system of Siboglinidae may have evolved from a ganglionated nervous system with a dorsal brain, as seen in most extant annelids. RESULTS: The intraepidermal nervous systems of four female Osedax spp. and the bone-eating O. priapus male were reconstructed in detail by a combination of immunocytochemistry, CLSM, histology and TEM. They all showed a simple nervous system composed of an anterior ventral brain, connected with anteriorly directed paired palp and gonoduct nerves, and four main pairs of posteriorly directed longitudinal nerves (2 ventral, 2 ventrolateral, 2 sets of dorso-lateral, 2 dorsal). Transverse peripheral nerves surround the trunk, ovisac and root system. The nervous system of Osedax resembles that of other siboglinids, though possibly presenting additional lateral and dorsal longitudinal nerves. It differs from most Sedentaria in the presence of an intraepidermal ventral brain, rather than a subepidermal dorsal brain, and by having an intraepidermal nerve cord with several plexi and up to three main commissures along the elongated trunk, which may comprise two indistinct segments. CONCLUSIONS: Osedax shows closer neuroarchitectural resemblance to Vestimentifera + Sclerolinum (= Monilifera) than to Frenulata. The intraepidermal nervous system with widely separated nerve cords, double brain commissures, double palp nerves and other traits found in Osedax can all be traced to represent ancestral states of Siboglinidae. A broader comparison of the nervous system and body regions across Osedax and other siboglinids allows for a reinterpretation of the anterior body region in the group

Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms.

Bacterial symbioses allow annelids to colonise extreme ecological niches, such as hydrothermal vents and whale falls. Yet, the genetic principles sustaining these symbioses remain unclear. Here, we show that different genomic adaptations underpin the symbioses of phylogenetically related annelids with distinct nutritional strategies. Genome compaction and extensive gene losses distinguish the heterotrophic symbiosis of the bone-eating worm Osedax frankpressi from the chemoautotrophic symbiosis of deep-sea Vestimentifera. Osedax's endosymbionts complement many of the host's metabolic deficiencies, including the loss of pathways to recycle nitrogen and synthesise some amino acids. Osedax's endosymbionts possess the glyoxylate cycle, which could allow more efficient catabolism of bone-derived nutrients and the production of carbohydrates from fatty acids. Unlike in most Vestimentifera, innate immunity genes are reduced in O. frankpressi, which, however, has an expansion of matrix metalloproteases to digest collagen. Our study supports that distinct nutritional interactions influence host genome evolution differently in highly specialised symbioses

Factors affecting the rare earth element compositions in massive sulfides from deep-sea hydrothermal systems

To reconstruct the evolution of ore-forming fluids and determine the physicochemical conditions of deposition associated with seafloor massive sulfides, we must better understand the sources of rare earth elements (REEs), the factors that affect the REE abundance in the sulfides, and the REE flux from hydrothermal fluids to the sulfides. Here, we examine the REE profiles of 46 massive sulfide samples collected from seven seafloor hydrothermal systems. These profiles feature variable total REE concentrations (37.2–4,092 ppb) and REE distribution patterns (LaCN/LuCN ratios = 2.00–73.8; (Eu/Eu*)CN ratios = 0.34–7.60). The majority of the REE distribution patterns in the sulfides are similar to those of vent fluids, with the sulfides also exhibiting light REE enrichment. We demonstrate that the variable REE concentrations, Eu anomalies, and fractionation between light REEs and heavy REEs in the sulfides exhibit a relationship with the REE properties of the sulfide-forming fluids and the massive sulfide chemistry. Based on the sulfide REE data, we estimate that modern seafloor sulfide deposits contain approximately 280 tons of REEs. According to the flux of hydrothermal fluids at mid-ocean ridges (MORs) and an average REE concentration of 3 ng/g in these fluids, hydrothermal vents at MORs alone transport more REEs (>360 tons) to the oceans over the course of just two years than the total quantity of REEs in seafloor sulfides. The excess REEs (i.e., the quantity not captured by massive sulfides) may be transported away from the systems and become bound in sulfate deposits and metalliferous sediments

High diversity in neuropeptide immunoreactivity patterns among three closely related species of Dinophilidae (Annelida).

This is the author accepted manuscript.The final version is available from Wiley via the DOI in this record.Neuropeptides are conserved metazoan signaling molecules, and represent useful markers for comparative investigations on the morphology and function of the nervous system. However, little is known about the variation of neuropeptide expression patterns across closely related species in invertebrate groups other than insects. In this study, we compare the immunoreactivity patterns of 14 neuropeptides in three closely related microscopic dinophilid annelids (Dinophilus gyrociliatus, D. taeniatus and Trilobodrilus axi). The brains of all three species were found to consist of around 700 somata, surrounding a central neuropil with 3-5 ventral and 2-5 dorsal commissures. Neuropeptide immunoreactivity was detected in the brain, the ventral cords, stomatogastric nervous system, and additional nerves. Different neuropeptides are expressed in specific, non-overlapping cells in the brain in all three species. FMRFamide, MLD/pedal peptide, allatotropin, RNamide, excitatory peptide, and FVRIamide showed a broad localization within the brain, while calcitonin, SIFamide, vasotocin, RGWamide, DLamide, FLamide, FVamide, MIP, and serotonin were present in fewer cells in demarcated regions. The different markers did not reveal ganglionic subdivisions or physical compartmentalization in any of these microscopic brains. The non-overlapping expression of different neuropeptides may indicate that the regionalization in these uniform, small brains is realized by individual cells, rather than cell clusters, representing an alternative to the lobular organization observed in several macroscopic annelids. Furthermore, despite the similar gross brain morphology, we found an unexpectedly high variation in the expression patterns of neuropeptides across species. This suggests that neuropeptide expression evolves faster than morphology, representing a possible mechanism for the evolutionary divergence of behaviors.Villum Fonde

Chemical composition of Fe-Mn nodules and host bottom sediments along the submeridional profile across the Brazil Basin

Sedimentation and ore formation were studied in sediments from nine stations located along the 24°W profile in the Brazil Basin of the Atlantic Ocean. Bottom sediments are represented by mio- and hemipelagic muds, which are variably enriched in hydrothermal iron and manganese oxyhydroxides. As compared to bottom sediments from other basins of the Atlantic Ocean, the sediments in study are marked by extremely high manganese contents (up to 1.33%) and maximal enrichment in Ce. It was shown that the positive Ce anomaly is related to REE accumulation on iron oxyhydroxides. Influence of hydrothermal source leads to decrease of Ce anomaly and LREE/HREE ratio. In reduced sediments preservation of positive Ce anomaly and/or its disappearance was observed after iron and manganese reduction. REE contents were determined for the first time in the Ethmodiscus oozes of the Brazil Basin. Ore deposits of the Brazil Basin are represented by ferromanganese crusts and ferromanganese nodules. Judging from contents of iron, manganese, REE, and other trace elements, these formations are ascribed to sedimentation (hydrogenic) deposits. They are characterized by a notable positive Ce anomaly in the REE pattern. Extremely high Ce content (up to 96% of total REE) was discovered for the first time in the buried nodules (Mn/Fe = 0.88)