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If the address matches an existing account you will receive an email with instructions to retrieve your username. Google Scholar. Find this author on PubMed. Search for more papers by this author. 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. 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.

The exploration of the deep sea in the last decades has led to the discovery of many new species with unique adaptations to extreme environments, raising important questions on their origin and evolution through geological time [ 1 , 2 ]. Osedax is a genus of marine worms that colonize the bones of marine vertebrates, mostly whales, sunken to the sea-floor [ 3 ]. It belongs to the Siboglinidae family of annelids that, as adults, lack mouth and digestive system and are nutritionally dependent on endosymbiotic bacteria [ 4 ].

Among siboglinids, Osedax has developed a unique metazoan—bacteria symbiosis that exploits the organic material sequestered within the bones of dead vertebrates as an energy source. The posterior body of Osedax penetrates into the bone using root-like structures figure 1 a , b. The root epithelium absorbs bone collagen and lipids, which are possibly metabolized by heterotrophic symbiotic bacteria that serve for Osedax nutrition [ 3 , 6 ].

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The anterior part of the body, the trunk, extends into the water and is crowned with respiratory palps [ 7 ]. Modern and fossil Osedax borings.

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Arrow indicates borings in j , k. Scale bars are 1 cm and scale meshes have spacing of 1 mm. Online version in colour. Osedax is a highly speciose clade, found at depths ranging from 21 to m, with a near global geographical distribution [ 8 , 9 ]. The origins and causes of this diversity are an unresolved aspect of its biology and evolution. Molecular age estimations suggest that either Osedax split from its siboglinid relatives approximately 45 Ma, possibly coincident with the origins of large archeocete cetaceans during the Eocene [ 3 , 8 ], or approximately Ma in the Cretaceous, when it could have lived on the bones of large marine Mesozic reptiles [ 8 , 10 ].

Only direct fossil evidence of the trace fossil left by Osedax worms can confirm which of these scenarios is correct, as it is unlikely for the soft-bodied animal itself to be preserved. The oldest Osedax traces known to date come from approximately 30 Myr whale and fish bones, indicating a generalist ability to thrive on different vertebrate substrates [ 11 , 12 ].

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Here, we show that Osedax colonized the bones of plesiosaurs and cheloniids in the Cretaceous, validating the hypothesis of a Mesozoic origin of the clade and we provide important implications for the evolution of the entire Siboglinidae family. Traces resembling those created by recent Osedax species were found on: i one isolated plesiosaur humerus from the Cenomanian approx. No invertebrate remains are associated with them. The bones were investigated using micro-computed tomography CT , a well-established method that allows the morphology of subsurface bone structures to be quantitatively described, providing their three-dimensional reconstruction [ 5 ] see the electronic supplementary material for details on the specimens, figure S1; geological setting; and analytical methods.

Digital removal of the matrix overlying the plesiosaur humerus revealed that Osedax bioerosion is concentrated in the centre of the bone figure 1 d. Two intact individual borings were identified on the periphery of the bioeroded area figure 1 d. The borings consist of circular surficial openings diameter 0. Similar borings were identified on the cheloniid fragments figure 1 i — k ; electronic supplementary material, figure S3.

The costal plate, even if heavily eroded, shows some intact borings. The largest example consists of a small circular surface opening diameter 0. The rib shows 15 small sub-circular holes that extend as long tubes into the bone, terminating in expanded irregular chambers electronic supplementary material, figure S3. These chambers are generally smaller than those identified on the plesiosaur skeleton table 1. Quantitative morphometrics of individual Osedax borings in fossil Mesozoic reptile bones this study compared with Osedax borings in Cenozoic fossil bones.

Osedax often colonize bones in such dense aggregations that the cavities formed by their root systems merge together under the bone surface [ 14 ]. Therefore, only cavities with a single borehole reflect the shape of the root system of an individual animal and are of particular diagnostic value [ 14 ].

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The tube section represents the trunk of Osedax , partially embedded within bone matrix in modern specimens [ 15 ], whereas the chamber represents the hole left by the ovisac and root structure figure 1 b , c. Although modern Osedax borings display a diverse range of morphologies [ 5 ], the combination of a narrow opening with laterally expansive irregular subsurface chambers are diagnostic features of Osedax activity [ 14 ].

How to get into bones: proton pump and carbonic anhydrase in Osedax boneworms. The skin of Osedax Siboglinidae, Annelida : an ultrastructural investigation of its epidermis. J Morphol. The Osedax Trophosome: Organization and Ultrastructure. Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms. ISME J. Postembryonic development of the bone-eating worm Osedax japonicus. Full-length transcriptome assembly from RNA-Seq data without a reference genome.

Nat Biotechnol. Pfam: the protein families database.

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Nucleic Acids Res. Katz S, Rouse GW. The reproductive system of Osedax Annelida, Siboglinidae : ovary structure, sperm ultrastructure, and fertilization mode. Invertebr Biol. Analysis and update of the human solute carrier SLC gene superfamily. Hum genomics.

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Mol Aspects Med. Proton-coupled oligopeptide transporter family SLC physiological, pharmacological and pathological implications.

SLC6 transporters: structure, function, regulation, disease association and therapeutics. Reimer RJ. SLC a functionally diverse family of organic anion transporters. Wright EM. Halestrap AP. The SLC16 gene family - structure, role and regulation in health and disease. Osteoclastic bone resorption by a polarized vacuolar proton pump. Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. Wada H. Origin and genetic evolution of the vertebrate skeleton. The evolution of the vertebrate metzincins; insights from Ciona intestinalis and Danio rerio.

Dev Biol. Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim Biophys Acta.

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Matrix remodeling during endochondral ossification. Trends Cell Biol. Insights into bilaterian evolution from three spiralian genomes. MMPs regulate both development and immunity in the tribolium model insect. Matrix metalloproteinase 2 is required for ovulation and corpus luteum formation in Drosophila. PLoS Genet.

The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem. Molecular cloning of human cDNA for cathepsin K: novel cysteine proteinase predominantly expressed in bone. Biochem Biophys Res Commun. Cathepsin B in osteoarthritis: zonal variation of enzyme activity in human femoral head cartilage.