Genetic mechanisms of bone digestion and nutrient absorption in the bone-eating worm Osedax japonicus inferred from transcriptome and gene expression analyses

Abstract

BackgroundBone-eating worms of the genus Osedax (Annelida, Siboglinidae) have adapted to whale fall environments by acquiring a novel characteristic called the root, which branches and penetrates into sunken bones. The worms lack a digestive tract and mouth opening, and it has been suggested that Osedax degrade vertebrate bones and uptake nutrients through acidification and secretion of enzymes from the root. Symbiotic bacteria in the root tissue may have a crucial role in the metabolism of Osedax. However, the molecular mechanisms and cells responsible for bone digestion and nutrient uptake are still unclear, and information on the metabolic interaction between Osedax and symbiotic bacteria is limited.ResultsWe compared transcriptomes from three different RNA samples from the following tissues: trunk + palps, root + ovisac, and larva + male. A Pfam domain enrichment analysis revealed that protease- and transporter-related genes were enriched in the root + ovisac specific genes compared with the total transcriptome. Through targeted gene annotation we found gene family expansions resulting in a remarkably large number of matrix metalloproteinase (mmp) genes in the Osedax compared with other invertebrates. Twelve of these Osedax mmp genes were expressed in the root epidermal cells. Genes encoding various types of transporters, including amino acid, oligopeptide, bicarbonate, and sulfate/carboxylate transporters, were also expressed in root epidermal cells. In addition, amino acid and other metabolite transporter genes were expressed in bacteriocytes. These protease and transporter genes were first expressed in root tissues at the juvenile stage, when the root starts to develop.ConclusionsThe expression of various proteinase and transporter genes in the root epidermis supports the theory that the root epidermal cells are responsible for bone digestion and subsequent nutrient uptake. Expression of transporter genes in the host bacteriocytes suggests the presence of metabolic interaction between Osedax and symbiotic bacteria.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0844-4) contains supplementary material, which is available to authorized users.

The Scaly-foot Snail genome and implications for the origins of biomineralised armour

“…To localize the expression of genes involved in scale and mantle formation, in situ hybridisation was performed on scale-secreting epidermis and the mantle of Scaly-foot Snails collected from the Solitaire field, fixed in 4% PFA solution and stored in 80% ethanol. In situ hybridisation was performed according to methods detailed in Miyamoto et al 75 with slight modifications, detailed as follows.…”

Pliocene stratigraphic paleobiology in Tuscany and the fossil record of marine megafauna

“…Whale-fall habitats likely undergo a temporal microbial succession from primarily heterotrophic to more heterotrophic/chemosynthetic metabolisms until the whale biomass is completely exploited (Smith et al, 2015). Of all the specialised taxa, bone-eating polychaetes of genus Osedax, with their soft root-like tissues that erode the bones to access nutrients (Tresguerres et al, 2013;Miyamoto et al, 2017), are the primary cause of bone disintegration, particularly of denser bones (Higgs et al, 2011). Found also at shelf depths, but invariably in low abundance (Huusgaard et al, 2012;Higgs et al, 2014b), bone-eating worms occur in high numbers in the deep sea (Smith et al, 2015) where they act as biodiversity regulators (Alfaro-Lucas et al, 2017).…”

“…Up to the Early-Late Cretaceous, biological activity is testified by circumstantial evidence of scavenging (Hybodus teeth associated with marine reptile skeletons, Martill et al, 1994), and by the more common occurrence of microbial mats, grazers and encrusters (Martill, 1987;Meyer, 2011;Reolid et al, 2015), but lack traces of bone-eating worms and sulphophilic fauna typical of modern whale falls. The siboglinid Osedax is an evolutionary novelty in possessing a root system that hosts heterotrophic mutualists and secretes bone-dissolving acids (Tresguerres et al, 2013;Miyamoto et al, 2017), and an ecosystem engineer (Alfaro-Lucas et al, 2017). Osedax is today associated with whale falls worldwide (Taboada et al, 2015), but its impact on MM has changed in time.…”

New species of bone-eating worm Osedax from the abyssal South Atlantic Ocean (Annelida, Siboglinidae)

“…Instead, female Osedax possesses a vascularised “root” system penetrating the bone marrow (Rouse et al 2004). Osedax worms are believed to acquire nutrition from the bones through their roots (Tresguerres et al 2013, Miyamoto et al 2017). Intracellular heterotrophic bacteria localise in the roots, but their role remains unclear (Goffredi et al 2014).…”