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

ABSTRACT: 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. 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.We 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.The 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.

SUBMITTER: Miyamoto N

PROVIDER: S-EPMC5237233 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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

Miyamoto Norio N Yoshida Masa-Aki MA Koga Hiroyuki H Fujiwara Yoshihiro Y

BMC evolutionary biology 20170113 1

<h4>Background</h4>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. 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 metabolis ...[more]

PMID: 28086748

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Project description:BACKGROUND:Bone-eating Osedax worms have proved to be surprisingly diverse and widespread. Including the initial description of this genus in 2004, five species that live at depths between 25 and 3,000 m in the eastern and western Pacific and in the north Atlantic have been named to date. Here, we provide molecular and morphological evidence for 12 additional evolutionary lineages from Monterey Bay, California. To assess their phylogenetic relationships and possible status as new undescribed species, we examined DNA sequences from two mitochondrial (COI and 16S rRNA) and three nuclear genes (H3, 18S and 28S rRNA). RESULTS:Phylogenetic analyses identified 17 distinct evolutionary lineages. Levels of sequence divergence among the undescribed lineages were similar to those found among the named species. The 17 lineages clustered into five well-supported clades that also differed for a number of key morphological traits. Attempts to determine the evolutionary age of Osedax depended on prior assumptions about nucleotide substitution rates. According to one scenario involving a molecular clock calibrated for shallow marine invertebrates, Osedax split from its siboglinid relatives about 45 million years ago when archeocete cetaceans first appeared and then diversified during the late Oligocene and early Miocene when toothed and baleen whales appeared. Alternatively, the use of a slower clock calibrated for deep-sea annelids suggested that Osedax split from its siboglinid relatives during the Cretaceous and began to diversify during the Early Paleocene, at least 20 million years before the origin of large marine mammals. CONCLUSION:To help resolve uncertainties about the evolutionary age of Osedax, we suggest that the fossilized bones from Cretaceous marine reptiles and late Oligocene cetaceans be examined for possible trace fossils left by Osedax roots. Regardless of the outcome, the present molecular evidence for strong phylogenetic concordance across five separate genes suggests that the undescribed Osedax lineages comprise evolutionarily significant units that have been separate from one another for many millions of years. These data coupled with ongoing morphological analyses provide a solid foundation for their future descriptions as new species.

Project description:Osedax, the deep-sea annelid found at sunken whalefalls, is known to host Oceanospirillales bacterial endosymbionts intracellularly in specialized roots, which help it feed exclusively on vertebrate bones. Past studies, however, have also made mention of external bacteria on their trunks. During a 14-yr study, we reveal a dynamic, yet persistent, shift of Campylobacterales integrated into the epidermis of Osedax, which change over time as the whale carcass degrades on the sea floor. The Campylobacterales associated with seven species of Osedax, which comprise 67% of the bacterial community on the trunk, appear initially dominated by the genus Arcobacter (at early time points <24 mo), the Sulfurospirillum at intermediate stages (~50 mo), and the Sulfurimonas at later stages (>140 mo) of whale carcass decomposition. Metagenome analysis of the epibiont metabolic capabilities suggests potential for a transition from heterotrophy to autotrophy and differences in their capacity to metabolize oxygen, carbon, nitrogen, and sulfur. Compared to free-living relatives, the Osedax epibiont genomes were enriched in transposable elements, implicating genetic exchange on the host surface, and contained numerous secretions systems with eukaryotic-like protein (ELP) domains, suggesting a long evolutionary history with these enigmatic, yet widely distributed deep-sea worms. IMPORTANCE Symbiotic associations are widespread in nature and we can expect to find them in every type of ecological niche. In the last twenty years, the myriad of functions, interactions and species comprising microbe-host associations has fueled a surge of interest and appreciation for symbiosis. During this 14-year study, we reveal a dynamic population of bacterial epibionts, integrated into the epidermis of 7 species of a deep-sea worm group that feeds exclusively on the remains of marine mammals. The bacterial genomes provide clues of a long evolutionary history with these enigmatic worms. On the host surface, they exchange genes and appear to undergo ecological succession, as the whale carcass habitat degrades over time, similar to what is observed for some free-living communities. These, and other annelid worms are important keystone species for diverse deep-sea environments, yet the role of attached external bacteria in supporting host health has received relatively little attention.

Project description:Osedax, commonly known as bone-eating worms, are unusual marine annelids belonging to Siboglinidae and represent a remarkable example of evolutionary adaptation to a specialized habitat, namely sunken vertebrate bones. Usually, females of these animals live anchored inside bone owing to a ramified root system from an ovisac, and obtain nutrition via symbiosis with Oceanospirillales gamma-proteobacteria. Since their discovery, 26 Osedax operational taxonomic units (OTUs) have been reported from a wide bathymetric range in the Pacific, the North Atlantic, and the Southern Ocean. Using experimentally deployed and naturally occurring bones we report here the presence of Osedax deceptionensis at very shallow-waters in Deception Island (type locality; Antarctica) and at moderate depths near South Georgia Island (Subantarctic). We present molecular evidence in a new phylogenetic analysis based on five concatenated genes (28S rDNA, Histone H3, 18S rDNA, 16S rDNA, and cytochrome c oxidase I-COI-), using Maximum Likelihood and Bayesian inference, supporting the placement of O. deceptionensis as a separate lineage (Clade VI) although its position still remains uncertain. This phylogenetic analysis includes a new unnamed species (O. 'mediterranea') recently discovered in the shallow-water Mediterranean Sea belonging to Osedax Clade I. A timeframe of the diversification of Osedax inferred using a Bayesian framework further suggests that Osedax diverged from other siboglinids during the Middle Cretaceous (ca. 108 Ma) and also indicates that the most recent common ancestor of Osedax extant lineages dates to the Late Cretaceous (ca. 74.8 Ma) concomitantly with large marine reptiles and teleost fishes. We also provide a phylogenetic framework that assigns newly-sequenced Osedax endosymbionts of O. deceptionensis and O. 'mediterranea' to ribospecies Rs1. Molecular analysis for O. deceptionensis also includes a COI-based haplotype network indicating that individuals from Deception Island and the South Georgia Island (ca. 1,600 km apart) are clearly the same species, confirming the well-developed dispersal capabilities reported in other congeneric taxa. In addition, we include a complete description of living features and morphological characters (including scanning and transmission electron microscopy) of O. deceptionensis, a species originally described from a single mature female, and compare it to information available for other congeneric OTUs.

Project description:Pancreatin secretion is dramatically decreased over time after weaning, thus affecting the utilization of nutrients in piglets. Therefore, exogenous pancreatin is expected to alleviate this situation. This experiment was conducted to investigate the effects of exogenous pancreatin on the growth performance, nutrient digestion and absorption, and intestinal microbiota of piglets. One hundred eighty piglets (Duroc × Landrace × Yorkshire, 40 days) were randomly allotted to three treatments (basal diets supplemented with 0, 250, or 500 mg/kg pancreatin) with three replicate pens per treatment and 20 piglets per pen. Compared with the control diet, dietary 500 mg/kg pancreatin significantly increased (p < 0.05) the average daily gain (ADG) and the apparent digestibility of crude protein and crude fat of piglets. Regarding endogenous enzymes, pancrelipase activity in the pancreas, duodenal mucosa, and small intestinal digesta as well as trypsin activity in the jejunal digesta were increased in piglets fed a diet supplemented with 500 mg/kg pancreatin (p < 0.05). Moreover, amylopsin activity was significantly strengthened in the pancreas, duodenal mucosa, and digesta in piglets fed a diet with 500 mg/kg pancreatin (p < 0.05). The mRNA expression of nutrient transporters, including oligopeptide transporter-1 (PepT1), excitatory amino acid transporter-1 (EAAC1), cationic amino acid transporter-1 (CAT1), sodium glucose cotransporter-1 (SGLT1), glucose transporter-2 (GLUT2), and fatty acid transporter-4 (FATP4), in the jejunum significantly increased after dietary supplementation with 500 mg/kg pancreatin (p < 0.05). An increased villus height-to-crypt depth ratio of the ileum was observed in the 500 mg/kg pancreatin-treated group (p < 0.05). The composition of the colonic microbiota modulated by the addition of 500 mg/kg pancreatin was characterized by an increased relative abundance of Lactobacillus (p < 0.05), and the predicted functions revealed that 500 mg/kg pancreatin supplementation enhanced the functional abundance of genetic information processing in colonic microorganisms and environmental information processing. Our findings suggested that the addition of 500 mg/kg pancreatin improved the growth performance of piglets, improved intestinal structure, and modulated the colon microbiota, thereby increasing nutrient digestibility.

Dataset Information

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

Publications

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

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