Not whale-fall specialists, Osedax worms also consume fishbones

Marine annelid worms of the genus Osedax exploit sunken vertebrate bones for food. To date, the named species occur on whale or other mammalian bones, and it is argued that Osedax is a whale-fall specialist. To assess whether extant Osedax species could obtain nutrition from non-mammalian resources, we deployed teleost bones and calcified shark cartilage at approximately 1000 m depth for five months. Although the evidence from shark cartilage was inconclusive, the teleost bones hosted three species of Osedax, each of which also lives off whalebones. This suggests that rather than being a whale-fall specialist, Osedax has exploited and continues to exploit a variety of food sources. The ability of Osedax to colonize and to grow on fishbone lends credibility to a hypothesis that it might have split from its siboglinid relatives to assume the bone-eating lifestyle during the Cretaceous, well before the origin of marine mammals.     

Molecular phylogeny of siboglinid annelids (a.k.a. pogonophorans): a review

Siboglinid, or pogonophoran, annelids are tubicolous worms that rely on chemoautotrophic endosymbionts for nutrition. Three clades within the siboglinids are recognized: Frenulata, Vestimentifera, and Monilifera. As a group, these worms have received considerable attention from molecular phylogenetists. Most studies have focused either on the evolutionary origins of the group or on the relationships within vestimentiferans, which live at hydrocarbon seeps and hydrothermal vents. Here I review the literature to date on siboglinid molecular phylogeny and summarize the clade’s evolution. The vestimentiferans have been well studied, especially in the eastern Pacific. The seep taxon Lamellibrachia is basal in the clade with vent species being more derived. Recent studies of seeps are finding new species and suggest that habitat depth can be correlated with species boundaries. In contrast to the vestimentiferans, frenulate evolution has been poorly studied. Despite their greater apparent diversity, frenulate specimens have not been sampled so extensively, and thus little is known about their evolution. Sclerolinum, also referred to as Monilifera, is a recognized genus of siboglinids that forms the sister group to Vestimentifera. Like the frenulates, little is known about the history of this group. Our present understanding of siboglinid phylogeny has, in large part, been dictated by insufficient sampling effort.     

Pogonophora (Annelida): form and function

Pogonophora, also known as Siboglinidae, are tube-dwelling marine annelids. They rely on endosymbiotic chemoautotrophic bacteria for nutrition and their anatomy and physiology are adapted to their need to obtain both oxygen and reduced sulphur compounds. Frenulate pogonophores are generally long and slender, sediment-living tubeworms; vestimentiferans are stouter, inhabitants of hydrothermal vents and cool seeps; and moniliferans or sclerolinids are very slender inhabitants of decaying wood and sulphidic sediments. The anatomy and ultrastructure of the three groups are compared and recent publications are reviewed. Annelid characters are the presence of chaetae and septa, concentrated at the hind end. The adaptations to a specialised way of life include, in particular, the chitinous tube; the anterior appendages that function as gills; the internal tissue called the trophosome, where the endosymbiotic bacteria live; and the blood vascular system that transports oxygen, sulphide and carbon dioxide to the trophosome.     

Bone-eating Osedax females and their 'harems' of dwarf males are recruited from a common larval pool

Extreme male dwarfism occurs in Osedax (Annelida: Siboglinidae), marine worms with sessile females that bore into submerged bones. Osedax are hypothesized to use environmental sex determination, in which undifferentiated larvae that settle on bones develop as females, and subsequent larvae that settle on females transform into dwarf males. This study addresses several hypotheses regarding possible recruitment sources for the males: (i) common larval pool--males and females are sampled from a common pool of larvae; (ii) neighbourhood--males are supplied by a limited number of neighbouring females; and (iii) arrhenotoky--males are primarily the sons of host females. Osedax rubiplumus were sampled from submerged whalebones located at 1820-m and 2893-m depths in Monterey Bay, California. Immature females typically did not host males, but mature females maintained male 'harems' that grew exponentially in the number of males as female size increased. Allozyme analysis of the females revealed binomial proportions of nuclear genotypes, an indication of random sexual mating. Analysis of mitochondrial DNA sequences from the male harems and their host females allowed us to reject the arrhenotoky and neighbourhood hypotheses for male recruitment. No significant partitioning of mitochondrial diversity existed between the male and female sexes, or between subsamples of worms collected at different depths or during different years (2002-2007). Mitochondrial sequence diversity was very high in these worms, suggesting that as many as 10(6) females contributed to a common larval pool from which the two sexes were randomly drawn.     

Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms

Deep-sea vestimentiferan tubeworms, which live in symbiosis with bacteria, exhibit different life strategies according to their habitat. At unstable and relatively short-lived hydrothermal vents, they grow extremely fast, whereas their close relatives at stable and long-persisting cold seeps grow slowly and live up to 300 years. Growth and age differences are thought to occur because of ecological and physiological adaptations. However, the underlying mechanisms of cell proliferation and death, which are closely linked to homeostasis, growth, and longevity, are unknown. Here, we show by immunohistochemical and ultrastructural cell cycle analyses that cell proliferation activities of the two species studied are higher than in any other characterized invertebrate, being only comparable with tumor and wound-healing processes. The slow growth in Lamellibrachia luymesi from cold seeps results from balanced activities of proliferation and apoptosis in the epidermis. In contrast, Riftia pachyptila from hydrothermal vents grows fast because apoptosis is down-regulated in this tissue. The symbiont-housing organ, the trophosome, exhibits a complex cell cycle and terminal differentiation pattern in both species, and growth is regulated by proliferation. These mechanisms have similarities to the up- and down-regulation of proliferation or apoptosis in various types of tumor, although they occur in healthy animals in this study, thus providing significant insights into the underlying mechanisms of growth and longevity. Financial support was provided by the Austrian Science Foundation (FWF; grants to M.B.), a DOC scholarship from the Austrian Academy of Science (to B.P.), and grants from the US National Science Foundation (to C.R. Fisher).     

Siboglinid evolution shaped by habitat preference and sulfide tolerance

Siboglinids are tube-dwelling annelids that inhabit marine reducing habitats such as anoxic mud bottoms, seeps and hydrothermal vents. As adults, they lack a functional digestive system and rely on chemoautotrophic microbial endosymbionts. Based on morphological analyses, Siboglinidae form a clade with the Sabellariidae, Serpulidae and Sabellidae within the Annelida. The sister group to this clade is the Oweniidae. Three subgroups constitute the Siboglinidae: Frenulata typically inhabit anoxic sediments, Sclerolinium (a.k.a., Monilifera) live on decaying organic matter or reduced sediments and Vestimentifera are mostly found at hydrocarbon seeps and hydrothermal vents. Recent studies suggest that Sclerolinum is the sister group to the Vestimentifera. Within the Vestimentifera, the species inhabiting bare-rock hydrothermal vents represent a derived clade. The seep-inhabiting genus Lamellibrachia forms a basal branch within the Vestimentifera. Trends in siboglinid evolution are most notable with regard to the level of sulfide tolerance and type of substrate. Basal groups inhabit soft substrate with only slightly elevated sulfide levels, whereas more derived species colonize hard substrate and tolerate elevated temperatures and high levels of sulfide. The type of substrate correlates with tube morphology and the function of the opisthosome. The role of the symbionts in habitat selection needs further investigation.     

Marine worms (genus Osedax) colonize cow bones

Bone-eating worms of the genus Osedax colonized and grew on cow bones deployed at depths ranging from 385 to 2893m in Monterey Bay, California. Colonization occurred as rapidly as two months following deployment of the cow bones, similar to the time it takes to colonize exposed whalebones. Some Osedax females found on the cow bones were producing eggs and some hosted dwarf males in their tubes. Morphological and molecular examinations of these worms confirmed the presence of six Osedax species, out of the eight species presently known from Monterey Bay. The ability of Osedax species to colonize, grow and reproduce on cow bones challenges previous notions that these worms are 'whale-fall specialists.'     

包埋法固定化对硫氧化微生物菌群结构和功能的影响

【目的】为探讨包埋法固定化过程对硫氧化菌群硫化物去除能力及菌群微生物群落结构的影响,【方法】以聚乙烯醇-海藻酸钠-活性炭为载体,对硫氧化菌群进行了固定化,并采用富含硫化物的无机盐培养基,对比固定化与非固定化硫氧化菌群对硫化物的氧化去除能力。同时,利用PCR-DGGE技术,探讨硫氧化菌群在固定化前后以及在硫化物氧化去除过程中微生物群落结构变化。【结果】在对硫氧化菌群进行固定化之后,12 h之内对硫化物的最大去除能力从1000 mg/L下降为600 mg/L。硫氧化菌群的微生物群落结构发生了明显变化,但菌群中的硫氧化菌Catenococcus thiocycli未受影响,硫氧化菌Thioclava pacifica在菌群中的地位反而得到了强化。【结论】受制于底物在载体材料中的扩散迁移效率,硫氧化菌群对硫化物的氧化去除能力在固定化之后有所下降。由于不同微生物对固定化形成的微环境的适应能力以及对载体附着能力的不同,固定化对硫氧化菌群的微生物群落结构产生较大影响。     

Carbon disulfide oxidation by a microbial consortium from a trickling filter

Biological oxidation rates of CS₂ with a mixed microbial culture obtained from a trickling filter were optimal with 3 mM CS₂, pH 7, 30°C and SO₄ ^2– below 25 g l^–1. Degradation rates were 3.4 mg CS₂/g_proteinmin and 13.8 mg H₂S/g_proteinmin. The concentrations of intermediates (H₂S, COS and S°) and the product (SO₄ ^2–) of CS₂ oxidation were measured. The biological oxidation was due principally to Gram negative bacteria.     

Bacterial Endosymbioses of Gutless Tube-Dwelling Worms in Nonhydrothermal Vent Habitats

Gutless tube-dwelling worms of pogonophorans (also known as frenulates) and vestimentiferans depend on primary production of endosymbiotic bacteria. The endosymbionts include thiotrophs that oxidize sulfur for autotrophic production and methanotrophs that oxidize and assimilate methane. Although most of the pogonophoran and vestimentiferan tube worms possess single thiotrophic 16S rRNA genes (16S rDNA) related to γ-proteobacteria, some pogonohorans are known to bear single methanotroph species or even dual symbionts of thiotrophs and methanotrophs. The vestimentiferan Lamellibrachia sp. L1 shows symbiotic 16S rDNA sequences of α-, β-, γ-, and ε-proteobacteria, varying among specimens, with RuBisCO form II gene (cbbM) sequences related to β-proteobacteria. An unidentified pogonophoran from the world’s deepest cold seep, 7326-m deep in the Japan Trench, hosts a symbiotic thiotroph based on 16S rDNA with the RuBisCO form I gene (cbbL). In contrast, a shallow-water pogonophoran (Oligobrachia mashikoi) in coastal Japan Sea has a methanotrophic 16S rDNA and thiotrophic cbbL, which may suggest the feature of type X methanotrophs. These observations demonstrate that pogonophoran and vestimentiferan worms have higher plasticity in bacterial symbioses than previously suspected.     

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).     

Molecular characterization of bacteria associated with the trophosome and the tube of Lamellibrachia sp., a siboglinid annelid from cold seeps in the eastern Mediterranean

Specimens of Lamellibrachia ( Annelida: Siboglinidae ) were recently discovered at cold seeps in the eastern Mediterranean. In this study, we have investigated the phylogeny and function of intracellular bacterial symbionts inhabiting the trophosome of specimens of Lamellibrachia sp. from the Amon mud volcano, as well as the bacterial assemblages associated with their tube. The dominant intracellular symbiont of Lamellibrachia sp. is a gammaproteobacterium closely related to other sulfide-oxidizing tubeworm symbionts. In vivo uptake experiments show that the tubeworm relies on sulfide for its metabolism, and does not utilize methane. Bacterial communities associated with the tube form biofilms and occur from the anterior to the posterior end of the tube. The diversity of 16S rRNA gene phylotypes includes representatives from the same divisions previously identified from the tube of the vent species Riftia pachyptila , and others commonly found at seeps and vents.     

Polyhedral inclusion bodies in cells of nitrosomonas spec

Polyhedral inclusion bodies were observed in cells of a Nitrosomonas species. They were present in growing cells as well as in resting cells. In thin sections their size was about 130 nm in growing cells and about 185 nm in diameter in resting cells. The bodies were commonly located in the nucleoplasm. They appeared to be bounded by a nonunit membrane and had a granular substructure.In thin sections about 70% of the exponentially grown cells and about 20% of the resting cells of the investigated strain showed 1–7 respectively 1–3 inclusion bodies.     

Myzostomida: A review of the phylogeny and ultrastructure

Myzostomids are minute, soft-bodied, marine worms associated with echinoderms since the Carboniferous. Due to their long history as host-specific symbionts, they have acquired a highly derived body plan that obscures their phylogenetic affinities to other metazoans. Because certain organs are serially arranged a closer relationship between polychaetes and myzostomids has repeatedly been discussion. We presented here a review on the ultrastructure of myzostomids with the most recent analyses that concern their phylogenetic position. The ultrastructure of the integument, digestive system, excretory system and nervous system are summarized. Unpublished information on the gametogenesis and reproductive systems of myzostomids are also exposed with a view on their reproductive process.     

Influence of the Cerebral Neuroendocrine System on Neutral Lipid Synthesis During Oogenesis in Nereis diversicolor (Annelida Polychaeta)

Summary

After brief incorporation with ³H-glycerol, neutral lipid synthesis is lower in coelomocytes from decerebrated worms than in coelomocytes from control worms, but later this relationship is reversed. The presence of the brain increases the synthesis of neutral lipid, especially triglycerides, by coelomo-cytes maintained in vitro. The release of triglycerides in vitro by previously labelled coelomocytes is also stimulated by cerebral endocrine factors.