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

Norio Miyamoto,Hiroyuki Koga,Yoshihiro Fujiwara,Masa-Aki Yoshida

doi:10.1186/s12862-016-0844-4

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.

Highlights

Bone-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
We set the threshold for gene expression intensity to eliminate fluctuations or background noise and 22,541 genes were found above the threshold in at least one sample
We examined the expression of 16 mmp genes and performed double staining with a probe against the 16S rRNA gene of Neptunomonas japonica (Nj 16S rRNA) infected with O. japonicus to clarify the localization of bacteriocytes harboring symbiotic bacteria

Summary

Introduction

Bone-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. Since the discovery of an invertebrate community in the Galapagos Rift in 1977 [1], several chemosynthetic ecosystems have been found in hydrothermal vents and hydrocarbon seeps worldwide [2, 3] In these environments, many endemic species, such as vestimentiferan tubeworms, vesicomyid clams, and Rimicaris shrimps, have been reported [2]. When a carcass of a large vertebrate (e.g., a whale) sinks to the sea floor, the huge source of organic material harbors a variety of organisms. Mobile scavengers such as sharks, hagfishes, and crustaceans aggregate and consume the soft tissue of the carcass [7]. After the bones of the carcass are exposed, enigmatic marine worms of the genus Osedax colonize on the bones [8]

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