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.     

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.     

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.     

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.     

Global diversity of polychaetes (Polychaeta; Annelida) in freshwater

A literature review of Polychaeta (Annelida) including Aphanoneura (the oligochaete-like Aeolosomatidae and Potamodrilidae), living in freshwater yielded 168 species, 70 genera and 24 families representing all of the major polychaete clades, but less than 2% of all species. The best-represented families were, in order, Nereididae, Aeolosomatidae, Sabellidae, Spionidae and Histriobdellidae. Fourteen families were represented by a single species and genus. Regions supporting the highest diversity of freshwater polychaetes were in order, Palaearctic, Neotropical, Oriental, Nearctic, Australasian, and Afrotropical. More than half of all species and genera inhabitat lakes and rivers, followed by lagoons/estuaries, which have a high proportion of euryhaline species, and inland seas. Less common, atypical polychaete habitats include subterranean waters, the hyporheic zone of rivers and plant container habitats (phytotelmata). At least three distinct ecological/historical processes appear to account for the colonisation of continental waters: invasion of a clade prior to the break-up of Gondwana, as in Aphanoneura, Namanereis, Stratiodrilus, and Caobangia; relatively recent stranding of individual species (relicts); and the temporary visitation of euryhaline species. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

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.     

A remarkable case of fiddler crab, Uca spp., alpha diversity in Wallacea

A preliminary attempt was made to quantify the alpha diversity of fiddler crabs (Uca spp.) along a short transect across the interface between an intertidal mudflat and a largely Avicennia mangrove at Ambeua on the Indonesian island of Kaledupa in Sulawesi Tenggara, by means of visual counts within 2 m² quadrats. An astounding diversity of up to six seemingly coexisting species per quadrat—and a total of seven such species within an area of 4 m²—was revealed. Four species of the ecologically equivalent sentinel crabs (Macrophthalmus) were also present in the quadrats. Seven fiddler crab species equates to more than half those known from Wallacea, more than one-third of all those known from Indonesia, and almost one-fifth of the entire Uca fauna of the Indo-West-Pacific.     

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.     

Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I

Naidids are tiny, primarily freshwater oligochaete annelids which reproduce asexually by fission. We investigated the phylogenetic relationships within this group by sequencing 1224 bp of the mitochondrial gene cytochrome oxidase I (COI) from 26 species of naidids (representing 13 of the 23 genera currently recognized), as well as from four tubificids, their closest allies. Although not completely concordant, maximum parsimony and Bayesian inference analyses agreed in several important respects, with no well-supported conflicts. Our study, the first detailed molecular investigation of naidid relationships, suggests that naidids fall into two groups, one comprised of the genus Pristina, and another comprised of all other genera sampled. The clear division of naidids into these two groups best matches an early, simple classification of the group by Lastockin (1924); the more recent classifications proposed by Sperber (1948) and Nemec and Brinkhurst (1987) are not as consistent with our results. We note that our study suggests the genus Stylaria is comprised of two distinct species, Stylaria lacustris and Stylaria fossularis, rather than merely two morphotypes of a single species. Based on our phylogenetic results, we suggest that pigmented eyes evolved only once among naidids but must have been lost multiple times, and that the elongation of the prostomium into a proboscis evolved at least twice independently. The simplest form of fission, architomy (fragmentation), occurs in two of the most basally branching naidid genera, and may represent the plesiomorphic condition for naidids.     

Observations on three species of branchiobdellid (Annelida: Clitellata) worms from eastern Asia

Three jars from the Hamburg Museum contained specimens of Branchiobdella minuta, presumably from the original Pierantoni (1912) material, and Cirrodrilus cirratus and C. uchidai from Yamaguchi's (1932a) collection. The head of a syntype of B. minuta was described and B. cheni becomes its junior subjective synonym. One specimen each of C. cirratus and C. uchidai was sectioned and described, particularly the male genitalia. The diet of all three branchiobdellids consists of microorganisms. In Cirrodrilus sp. basic protein granules were demonstrated in the gland cells of the intestine and its chloragogen cells. The peristomial and lateral epidermal gland cell secretions were characterized histochemically.     

The phylogeny of Branchiobdellida (Annelida, Clitellata) assessed by sperm characters

Data on the spermatozoa of Branchiobdellida were taken from the published literature: sperm models of 25 species belonging to 13 different branchiobdellidan genera have been compared with the aim of supplying further evidences for a phylogenetic analysis of the group. The species considered were representative of all traditional branchiobdellidan families, excluding the monotypic Caridinophilidae. Branchiobdellidan spermatozoa are complex cells, thus it was possible to analyse the variation of 20 characters within the group. A parsimony analysis has yielded nine minimal trees, eight of which are very similar to one another. The main conclusions of the phylogenetic analysis are: (a) the monophyly of the taxon Branchiobdellida is confirmed; (b) the most speciose branchiobdellidan genus, Cambarincola is polyphyletic; (c) none of the traditional ‘families’ are supported; (d) the genus Branchiobdella is monophyletic, but the position of one species, B. kobayashi, albeit basal to the whole genus, is not resolved; (e) the other two genera analysed for which more than one species was available, Pterodrilus and Xironogiton, are monophyletic; (f) there seems to be a ‘trend’ in the whole group towards an increase of acrosome length. Our results partly parallel those obtained by Gelder and Siddall (2000) with a combined analysis of molecular and somatic characters, and point to the need for a comprehensive revision of the Branchiobdellida based on a combination of molecular, somatic and spermatological data sets.     

Questa (Annelida, Polychaeta, Orbiniidae) from Pacific regions — new species and reassessment of the genus Periquesta

On the basis of new material from various Pacific regions we critically evaluate the characters for the taxonomy of the genus Questa and the former Questidae, a taxon now concluded to be a lineage within the family Orbiniidae. Two new species, Questa retrospermatica sp. n. from Hawaii (with similar forms also from New Caledonia and China), and Questa fijiensis sp. n. from Fiji, are described, and the morphological character patterns and phylogeny of the genus are revisited on the basis of a cladistic analysis. The finding of Hawaiian material of a new species, Levinsenia hawaiiensis sp. n., similar to Periquesta canariensis Brito & Nunez, 2002 (=Levinsenia canariensis comb. n.), challenges the view that Periquesta Brito & Nunez, 2002 is closely related to Questa; rather, it belongs to Paraonidae as a junior synonym of Levinsenia Mesnil, 1897.     

Microstructure and formation of the calcareous operculum in Pyrgopolonctenactis and Spirobranchusgiganteus (Annelida, Serpulidae)

The calcareous operculum of Pyrgopolon ctenactis is composed of spherulitic prismatic structures. The opercular cup consists of regular spherulitic prismatic crystals; the talon has two layers, an inner with an irregular spherulitic prismatic structure (150 μm thick) and an outer with a regular spherulitic prismatic structure (110 μm thick). The outer regular structure has thick (1 μm) organic interprismatic sheets unique in biomineralization of this group, but similar to that of Bivalvia. We infer that control over biomineralization is stronger during the formation of the outer regular layer, with its thick organic interprismatic sheets, than during the formation of the inner irregular spherulitic prismatic structure, without such sheets. In Spirobranchus giganteus, opercular formation differs from that of P. ctenactis. S. giganteus has numerous pores in its opercular plate, and calcification starts with the formation of an outer irregularly oriented prismatic structure followed by an oriented prismatic structure without interprismatic sheets.     

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.