A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida)

Background

We previously showed that mice lacking the high mobility group A1 gene (Hmga1-knockout mice) developed a type 2-like diabetic phenotype, in which cell-surface insulin receptors were dramatically reduced (below 10% of those in the controls) in the major targets of insulin action, and glucose intolerance was associated with increased peripheral insulin sensitivity. This particular phenotype supports the existence of compensatory mechanisms of insulin resistance that promote glucose uptake and disposal in peripheral tissues by either insulin-dependent or insulin-independent mechanisms. We explored the role of these mechanisms in the regulation of glucose homeostasis by studying the Hmga1-knockout mouse model. Also, the hypothesis that increased insulin sensitivity in Hmga1-deficient mice could be related to the deficit of an insulin resistance factor is discussed.

Results

We first show that HMGA1 is needed for basal and cAMP-induced retinol-binding protein 4 (RBP4) gene and protein expression in living cells of both human and mouse origin. Then, by employing the Hmga1-knockout mouse model, we provide evidence for the identification of a novel biochemical pathway involving HMGA1 and the RBP4, whose activation by the cAMP-signaling pathway may play an essential role for maintaining glucose metabolism homeostasis in vivo, in certain adverse metabolic conditions in which insulin action is precluded. In comparative studies of normal and mutant mice, glucagon administration caused a considerable upregulation of HMGA1 and RBP4 expression both at the mRNA and protein level in wild-type animals. Conversely, in Hmga1-knockout mice, basal and glucagon-mediated expression of RBP4 was severely attenuated and correlated inversely with increased Glut4 mRNA and protein abundance in skeletal muscle and fat, in which the activation state of the protein kinase Akt, an important downstream mediator of the metabolic effects of insulin on Glut4 translocation and carbohydrate metabolism, was simultaneously increased.

Conclusion

These results indicate that HMGA1 is an important modulator of RBP4 gene expression in vivo. Further, they provide evidence for the identification of a novel biochemical pathway involving the cAMP-HMGA1-RBP4 system, whose activation may play a role in glucose homeostasis in both rodents and humans. Elucidating these mechanisms has importance for both fundamental biology and therapeutic implications.     

A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan

A new whale-bone-eating polychaete species of the genus Osedax was found on sperm whale carcasses submerged off Cape Nomamisaki, Kyushu, Japan, at a depth of approximately 200 m. The new species, Osedax japonicus, is the fourth known species of the genus Osedax and the first species from the western Pacific. Female O. japonicus specimens (1) form dense clusters on whale carcasses; (2) have a body composed of crown, trunk, and root structure; (3) lack a digestive tract; and (4) have bacterium-like particles in the tissue of the root structure. Osedax japonicus shares all these characteristics with O. rubiplumus and O. frankpressi, and items (1) to (3) with O. mucofloris. Osedax japonicus is easily distinguished from the other three known species by oviduct morphology, body length, and palp coloration in females. No males of O. japonicus have yet been found.     

Bone-boring worms: characterizing the morphology, rate, and method of bioerosion by Osedax mucofloris (Annelida, Siboglinidae)

Osedax worms possess unique "root" tissues that they use to bore into bones on the seafloor, but details of the boring pattern and processes are poorly understood. Here we use X-ray micro-computed tomography to investigate the borings of Osedax mucofloris in bones of the minke whale (Balaenoptera acutorostrata), quantitatively detailing their morphological characteristics for the first time. Comparative thin-sections of the borings reveal how the bone is eroded at the sub-millimeter level. On the basis of these results we hypothesize a model of boring that is dependent on the density and microstructure of the bone. We also present evidence of acidic mucopolysaccharides in the mucus of the root tissue, and hypothesize that this plays an important role in the boring mechanism. We discuss the utility of these new data in evaluating Osedax trace fossils and their relevance for O. mucofloris ecology. Measured rates of bone erosion (6% per year) and evidence of enhanced sulfide release from the borings indicate that Osedax worms are important habitat modifiers in whale-fall communities.     

Protonephridial Excretory System in Vestimentifera (Siboglinidae,Annelida)

Ultrastructural study of the excretory tree of vestimentifera Ridgeia piscesae has shown that it consists of tubules that are blind at their distal ends. The tubules are lined with ciliated cells and have one or two multiciliated terminal cell(s) at the distal ends. In the tubule walls, there are putative ultrafiltration sites. The excretory tree tubules are interpreted as the secondary protonephridia.     

Acquisition of dwarf male "harems" by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida)

After the deployment of several whale carcasses in Monterey Bay, California, a time-series analysis revealed the presence of a new species of Osedax, a genus of bone-eating siboglinid annelids. That species is described here as Osedax roseus n. sp. It is the fifth species described since the erection of this genus and, like its congeners, uses a ramifying network of "roots" to house symbiotic bacteria. In less than 2 months, Osedax roseus n. sp. colonized the exposed bones of a whale carcass deposited at 1018-m depth, and many of the females were fecund in about 3 months post-deployment. As with other Osedax spp., the females have dwarf males in their tube lumens. The males accrue over time until the sex ratio is markedly male-biased. This pattern of initial female settlement followed by gradual male accumulation is consistent with the hypothesis that male sex may be environmentally determined in Osedax. Of the previously described species in this genus, Osedax roseus n. sp. is most similar to O. rubiplumus, but it has several anatomical differences, as well as much smaller females, dwarf males, and eggs. Osedax roseus n. sp. is markedly divergent (minimally 16.6%) for mitochondrial cytochrome oxidase subunit I (mtCOI) sequences from any other Osedax species.     

Endosymbionts of Siboglinum fiordicum and the phylogeny of bacterial endosymbionts in Siboglinidae (Annelida)

Siboglinid worms are a group of gutless marine annelids that are nutritionally dependent upon endosymbiotic bacteria. Four major groups of siboglinids are known-vestimentiferans, moniliferans, Osedax spp. and frenulates. Although endosymbionts of vestimentiferans and Osedax spp. have been previously characterized, little is currently known about endosymbiotic bacteria associated with frenulate and moniliferan siboglinids. This is particularly surprising given that frenulates are the most diverse and widely distributed group of siboglinids. Here, we molecularly characterize endosymbiotic bacteria associated with the frenulate siboglinid Siboglinum fiordicum by using 16S rDNA ribotyping in concert with laser-capture microdissection (LCM). Phylogenetic analysis indicates that at least three major clades of endosymbiotic gamma-proteobacteria associate with siboglinid annelids, with each clade corresponding to a major siboglinid group. S. fiordicum endosymbionts are a group of gamma-proteobacteria that are divergent from bacteria associated with vestimentiferan or Osedax hosts. Interestingly, symbionts of S. fiordicum, from Norway, are most closely related to symbionts of the frenulate Oligobrachia mashikoi from Japan, suggesting that symbionts of frenulates may share common evolutionary history or metabolic features.     

The Composition,Structure, and Distribution of Benthic Ostracod Fauna (Ostracoda: Myodocopida) in Subantarctic Waters

Russian Journal of Marine Biology - This paper presents an analysis of the literature data on the Subantarctic fauna of the benthic Myodocopida, including 97 species. The studied fauna is...     

Impact of temperature on UV-susceptibility of two Ulva (Chlorophyta) species from Antarctic and Subantarctic regions

The interactive effects of UV-B-exposure and increased temperature were investigated in the two green macroalgae Ulva bulbosa from Antarctica and Ulva clathrata from southern Chile in the laboratory. At seawater temperatures of 0°C, UV-induced inhibition of photosynthesis was much larger in U. clathrata than in U. bulbosa, whereas temperatures of 10°C compensated UV-effects in both species. Despite pronounced photoinhibition, damage to D1 protein in photosystem II could not be detected, indicating that photosynthetic reaction centers were unaffected by experimental UV-exposure. In addition, marked differences in the generation of oxidative stress were not detected. Under all treatments, the activity of superoxide dismutase was higher in U. bulbosa than in U. clathrata, indicating a higher degree of cold adaptation in U. bulbosa from Antarctica, resulting in a higher UV-tolerance at 0°C than in U. clathrata from southern Chile.     

Molecular evidence that Sclerolinum brattstromi is closely related to vestimentiferans, not to frenulate pogonophorans (Siboglinidae, Annelida)

Siboglinids, previously referred to as pogonophorans, have typically been divided into two groups, frenulates and vestimentiferans. Adults of these marine protostome worms lack a functional gut and harbor endosymbiotic bacteria. Frenulates usually live in deep, sedimented reducing environments, and vestimentiferans inhabit hydrothermal vents and sulfide-rich hydrocarbon seeps. Taxonomic literature has often treated frenulates and vestimentiferans as sister taxa. Sclerolinum has traditionally been thought to be a basal siboglinid that was originally regarded as a frenulate and later as a third lineage of siboglinids, Monilifera. Evidence from the 18S nuclear rDNA gene and the 16S mitochondrial rDNA gene presented here shows that Sclerolinum is the sister clade to vestimentiferans although it lacks the characteristic morphology (i.e., a vestimentum). The rDNA data confirm the contention that Sclerolinum is different from frenulates, and further supports the idea that siboglinid evolution has been driven by a trend toward increased habitat specialization. The evidence now available indicates that vestimentiferans lack the molecular diversity expected of a group that has been argued to have Silurian or possibly Cambrian origins.     

Molecular Phylogeny of Echiuran Worms (Phylum: Annelida) Reveals Evolutionary Pattern of Feeding Mode and Sexual Dimorphism

The Echiura, or spoon worms, are a group of marine worms, most of which live in burrows in soft sediments. This annelid-like animal group was once considered as a separate phylum because of the absence of segmentation, although recent molecular analyses have placed it within the annelids. In this study, we elucidate the interfamily relationships of echiuran worms and their evolutionary pattern of feeding mode and sexual dimorphism, by performing molecular phylogenetic analyses using four genes (18S, 28S, H3, and COI) of representatives of all extant echiuran families. Our results suggest that Echiura is monophyletic and comprises two unexpected groups: [Echiuridae+Urechidae+Thalassematidae] and [Bonelliidae+Ikedidae]. This grouping agrees with the presence/absence of marked sexual dimorphism involving dwarf males and the paired/non-paired configuration of the gonoducts (genital sacs). Furthermore, the data supports the sister group relationship of Echiuridae and Urechidae. These two families share the character of having anal chaetae rings around the posterior trunk as a synapomorphy. The analyses also suggest that deposit feeding is a basal feeding mode in echiurans and that filter feeding originated once in the common ancestor of Urechidae. Overall, our results contradict the currently accepted order-level classification, especially in that Echiuroinea is polyphyletic, and provide novel insights into the evolution of echiuran worms.     

New alluroidids (Annelida,Clitellata) from Guyana

A total of 30 microbialites at two sites in Lake Clifton, Yalgorup National Park, Western Australia, were sampled by coring to quantify the associated fauna with these organo-sedimentary structures. Twenty five species of aquatic fauna were recorded from the cores, comprising 20 species of metazoan, predominantly Crustacea (including Melita kauerti (Amphipoda), Exosphaeroma cf. serventii (Isopoda); and Cyprideis australiensis(Ostracoda); Polychaeta (Capitella cf. capitata); nematodes; and five species of Foraminifera (Protista). Multivariate analysis of the five numerically most abundant taxa (amphipods, isopods, ostracods, polychaetes, nematodes) separated microbialites by season and submergence. Numbers of all taxa, particularly polychaetes and amphipods, were much higher in spring than in autumn, and in permanently-inundated than in seasonally-inundated microbialites. The exception was higher numbers of juvenile polychaetes in seasonally-inundated microbialites at the northern site in spring. This study showed that modern thrombolitic microbialites can co-exist with a diverse invertebrate fauna and serves as a baseline for future studies of interactions between microbialites and fauna.     

Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters

Colossendeis megalonyx Hoek, 1881 is a widespread and abundant pycnogonid in the Southern Ocean which has also been reported from the South Atlantic and South Pacific Oceans. Its strictly benthic lifestyle is expected to promote genetic differentiation among populations and ultimately facilitate speciation. On the other hand, the reported eurybathy and unknown larval stages of this species may allow Colossendeis megalonyx to maintain genetic continuity between isolated shallow-water habitats by active dispersal through the deep sea or by passive rafting on floating substrates. Thus, it remains unknown whether and to which extent geographically separated populations of Colossendeis megalonyx maintain gene flow in the Southern Ocean. We sampled 96 specimens of Colossendeis megalonyx from three stations in the Atlantic Sector of the Southern Ocean and one station from the South American continental shelf (Burdwood Bank). The genetic structure of nominal Colossendeis megalonyx as well as its phylogenetic position within the genus Colossendeis were assessed using a fragment of the cytochrome c oxidase subunit 1 gene. Our data strongly support that nominal Colossendeis megalonyx consists of at least five cryptic and one pseudocryptic mitochondrial lineages, four of which appear to be geographically restricted. Two lineages occurred at locations separated by more than 1,000 km in the Antarctic, thus indicating high levels of gene flow or recent colonization. No haplotype sharing across the Polar Frontal Zone was observed. Our results strongly suggest that cryptic speciation occurred within the genus Colossendeis. The wide biogeographic distribution range of Colossendeis megalonyx and perhaps that of other Antarctic pycnogonids should therefore be regarded with caution.     

Actual distribution of bacteriocytes in the trophosome of a beard worm (Oligobrachia mashikoi, Siboglinidae, Annelida): clarification using whole-mount in situ hybridization

Beard worms (Siboglinidae, Polychaeta) lack a mouth and a digestive tract and harbour chaemosynthetic bacteria in the bacteriocytes of the trophosome. Since beard worms depend on the organic compounds produced by the bacteria for nourishment, the bacteriocytes should be efficient in exchanging various substances with body fluids. For this reason, it is important to determine how the bacteriocytes are organized in the trophosome. As the first step of the present study, the appearance of bacteriocytes was examined in routinely stained paraffin sections. Second, visualization of the actual distribution of the bacteriocytes was attempted using whole‐mount in situ hybridization with a probe of the 16S rRNA nucleotide sequence of the bacterium. After routine haematoxylin & eosin staining, the bacteriocytes appeared to be aligned in cell cords accompanied with nutrient‐deposit cells that extended from both sides of the trophosome toward the dorsal side and folded up in the coelomic spaces. In whole‐mount preparations, however, bacteriocytes with intense signals of 16S rRNA were seen three‐dimensionally as many irregular leaves arranged from both sides of the ventral vessel toward the dorsal vessel. We will discuss the physiological significance of this characteristic distribution of the bacteriocytes in the present species.     

Occurrence of Diopatra marocensis (Annelida,Onuphidae) in the eastern Mediterranean

The present study deals with the presence of Diopatra marocensis in the eastern Mediterranean. This species is small-sized and inhabited muddy bottom near the opening of rivers or lagoons [salinity range: 33−39‰] in the Aegean and Levantine Seas, and reached a maximum density of 90 ind.m^-2 in Mersin Bay. This species might be an alien species that was introduced from the East Atlantic (near Gibraltar) to the eastern Mediterranean via ballast water of ships, as it has never been reported from the western Mediterranean Sea.     

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

Doklady Biological Sciences - 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...