Evidence of<i>Osedax</i>worm borings in Pliocene (∼3 Ma) whale bone from the Mediterranean

Higgs, Nicholas D.; Little, Crispin T. S.; Glover, Adrian G.; Dahlgren, Thomas G.; Smith, Craig R.; Dominici, Stefano

doi:10.1080/08912963.2011.621167

Cited by 31 publications

(73 citation statements)

References 38 publications

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“…Since Osedax do not have any obvious bioabrasive structures, Katz et al [14,15] suggested Osedax bored into bones by secreting acid. This possibility was also discussed by Higgs et al [16], who additionally found acidic mucopolysaccharides in the mucus of the root tissue and proposed that this material is important in the boring mechanism by acting as a chelating agent. However, the specific mechanisms by which Osedax secretes acid remain unknown.…”

Section: Introductionmentioning

confidence: 79%

“…The dual 'drilling and feeding' function does not occur in the boring invertebrate animals mentioned earlier, but it is analogous to the mechanism for bone resorption in osteoclast cells of vertebrate animals [18]. The potential similarities between marine boring organisms and osteoclasts have previously been recognized for sponges [8] and snails [10], and also Osedax [16].…”

Section: Introductionmentioning

confidence: 98%

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How to get into bones: proton pump and carbonic anhydrase inOsedaxboneworms

2013

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Osedax are gutless siboglinid worms that thrive on vertebrate bones lying on the ocean floor, mainly those of whales. The posterior body of female Osedax penetrates into the bone forming extensions known as 'roots', which host heterotrophic symbiotic bacteria in bacteriocytes beneath the epidermis. The Osedax root epithelium presumably absorbs bone collagen and/or lipids, which are metabolized by the symbiotic bacteria that in turn serve for Osedax's nutrition. Here, we show that Osedax roots express extremely high amounts of vacuolar-H þ -ATPase (VHA), which is located in the apical membrane and in cytoplasmic vesicles of root and ovisac epithelial cells. The enzyme carbonic anhydrase (CA), which catalyses the hydration of CO 2 into H þ and HCO 3 2 , is also expressed in roots and throughoutOsedax body. These results suggest Osedax roots have massive acid-secreting capacity via VHA, fuelled by H þ derived from the CA-catalysed hydration of CO 2 produced by aerobic metabolism. We propose the secreted acid dissolves the bone carbonate matrix to then allow the absorption of bonederived nutrients across the skin. In an exciting example of convergent evolution, this model for acid secretion is remarkably similar to mammalian osteoclast cells. However, while osteoclasts dissolve bone for repairing and remodelling, the Osedax root epithelium secretes acid to dissolve foreign bone to access nutrients.

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Section: Introductionmentioning

confidence: 79%

Section: Introductionmentioning

confidence: 98%

How to get into bones: proton pump and carbonic anhydrase inOsedaxboneworms

2013

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“…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]. 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 1b,c).…”

Section: Resultsmentioning

confidence: 99%

“…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].…”

Section: Resultsmentioning

confidence: 99%

Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls

Danise

Higgs

2015

Biol. Lett.

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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).

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“…Now, 17 morphologically diverse species are known worldwide from depths ranging from 25 to 3000 meters Rouse et al, 2004;Glover et al, 2005;Fujikura et al, 2006;Braby et al, 2007;Vrijenhoek et al, 2009;Salathé and Vrijenhoek, 2012). Evidence for Osedax borings in fossilized bones suggests that the genus has historically colonized a large portion of the world's oceans (Higgs et al, 2011;Kiel et al, 2011;Higgs et al, 2012). Much is now known about the role of these worms in degrading sunken bones and the recycling of deep-sea carbon (Goffredi et al, 2005;Braby et al, 2007), their phylogenetic relationships (Vrijenhoek et al, 2009;Hilário et al, 2011), and an unusual reproductive strategy that involves dwarf males and environmental sex determination Vrijenhoek et al, 2008;Rouse et al, 2011;Miyamoto et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

Goffredi

Zhang

et al. 2013

The ISME Journal

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An unusual symbiosis, first observed at B3000 m depth in the Monterey Submarine Canyon, involves gutless marine polychaetes of the genus Osedax and intracellular endosymbionts belonging to the order Oceanospirillales. Ecologically, these worms and their microbial symbionts have a substantial role in the cycling of carbon from deep-sea whale fall carcasses. Microheterogeneity exists among the Osedax symbionts examined so far, and in the present study the genomes of the two dominant symbionts, Rs1 and Rs2, were sequenced. The genomes revealed heterotrophic versatility in carbon, phosphate and iron uptake, strategies for intracellular survival, evidence for an independent existence, and numerous potential virulence capabilities. The presence of specific permeases and peptidases (of glycine, proline and hydroxyproline), and numerous peptide transporters, suggests the use of degraded proteins, likely originating from collagenous bone matter, by the Osedax symbionts. 13 C tracer experiments confirmed the assimilation of glycine/ proline, as well as monosaccharides, by Osedax. The Rs1 and Rs2 symbionts are genomically distinct in carbon and sulfur metabolism, respiration, and cell wall composition, among others. Differences between Rs1 and Rs2 and phylogenetic analysis of chemotaxis-related genes within individuals of symbiont Rs1 revealed the influence of the relative age of the whale fall environment and support possible local niche adaptation of 'free-living' lifestages. Future genomic examinations of other horizontally-propogated intracellular symbionts will likely enhance our understanding of the contribution of intraspecific symbiont diversity to the ecological diversification of the intact association, as well as the maintenance of host diversity.

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Evidence ofOsedaxworm borings in Pliocene (∼3 Ma) whale bone from the Mediterranean

Cited by 31 publications

References 38 publications

How to get into bones: proton pump and carbonic anhydrase inOsedaxboneworms

How to get into bones: proton pump and carbonic anhydrase inOsedaxboneworms

Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

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