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Osedax

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Osedax
Temporal range: Albian–Present
Osedax roseus
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Annelida
Clade: Pleistoannelida
Clade: Sedentaria
Order: Sabellida
Family: Siboglinidae
Genus: Osedax
Rouse et al., 2004[1]
Species

See text.

Osedax is a genus of deep-sea siboglinid polychaetes, commonly called boneworms, zombie worms, or bone-eating worms. Osedax is Latin for "bone-eater". The name alludes to how the worms bore into the bones of whale carcasses to reach enclosed lipids, on which they rely for sustenance. They utilize specialized root tissues for bone-boring. It is possible that multiple species of Osedax reside in the same bone.[2] Osedax worms are also known to feed on the collagen itself by making holes in the whale's skeletal structure. These holes can also serve as a form of protection from nearby predators.

Scientists from the Monterey Bay Aquarium Research Institute using the submarine ROV Tiburon first discovered the genus in Monterey Bay, California, in February 2002. The worms were found living on the bones of a decaying gray whale in the Monterey Canyon, at a depth of 2,893 m (9,491 ft).

Anatomy and physiology

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Osedax are colorful tubeworms that have no mouth, anus, or gut.[3] The body is divided into different regions: trunk, ovisac, and root. They range in length between 2.5 to 7 cm (0.98 to 2.76 in), although this varies between species (cite).[4] Sexual dimorphism is observed in Osedax with females >20,000 times larger than males.[5]

Digestive system

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Osedax rely on symbiotic species of bacteria that aid in the digestion of whale proteins and lipids and release nutrients that the worms can absorb.[6] Osedax have colorful feathery plumes that also act as gills and unusual root-like structures that absorb nutrients. The Osedax secrete acid (rather than rely on teeth) to bore into bone to access the nutrients.[7] High concentrations of carbonic anhydrase are found in the roots of Osedax. This serves as evidence of a common bioerosion mechanism in which secreted acid is produced by anaerobic respiration. This process works with a demineralization mechanism in which oxygen is carried from seawater to the roots and HCO−
3  is secreted into the seawater.[8]

The epidermis also plays key roles in bone deterioration and nutrient uptake. This process of bone deterioration occurs through a symbiotic relationship with an endosymbiotic bacteria.[9] The cells in the epidermis of the Osedax root region are responsible for the secretion of digestive enzymes. The epidermis also has an expanded microvillus border which increases the surface area.[9]

Through the use of X-ray CT technology, scans showed that borings made by Osedax mucofloris were hemi-ellipsoidal in shape. Boring depths varied depending on which bone was colonized by the O. mucofloris. Deeper borings were found in radius bone compared to the ulna and vertebrae.[10]

Osedax roots are covered by a mucus sheath that helps protect the worm's trunk. Some studies support the theory that this sheath plays a role in dissolving the bone. This sheath could also play an important role in reducing the damage to Osedax skin by absorbing harmful acid. Another potential function of the mucus sheath is that it could inhibit the breakdown of the worm's bone matrix. This is significant because the bone matrix is integral in maintaining the worm's position while in direct contact with a bone.[8]

Sexual dimorphism

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Osedax males are notably smaller than their female counterparts. Between 50 and 100 microscopic dwarf males live inside the tube surrounding a single female and never develop past the larval stage; they produce sperm from yolk reserves.[5] Male dwarfism prevents competition with female Osedax worms for food and space.[5] Conditions that favour dwarfism in male Osedax are:

  1. Eliminates competition between male and female Osedax as resources are limited,[11]
  2. Sessile lifestyle: attach to and rely on females for food,[11]
  3. Decreases difficulty in finding a mate.[11]

Interestingly, Osedax priapus lack the frequently observed male dwarfism. Males live freely and compete for space and food with females. Being larger, they produce and carry more sperm. However, sexual size dimorphism is still observed in O. priapus: most males are one-third the volume of females.[5]

Reproduction

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Discoveries

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Female Osedax worms have been observed spawning both in the wild and in laboratory aquaria.[12] Osedax rubiplumus can spawn hundreds of oocytes at a time. They are already fertilized when they are released from the female worm. The worms' endosymbionts, species of bacteria in the order Oceanospirillales, were not observed in the spawned oocytes, which suggests that they are acquired after the worms settle on the bones.[12] In the adult, the bacteria are localised in the root-like structures that grow into the whale bone.[13][14] This worm appears to be highly fecund and reproduces continuously. This may help explain why Osedax is such a diverse genus, despite the rarity of whale falls in the ocean.

Male Osedax are microscopic dwarfs that live as "harems" inside the lumen of the gelatinous tube that surrounds each female. An individual female can house hundreds of these males in her tube.[15][16]

Following its discovery in 2002 by researchers at the Monterey Bay Aquarium Research Institute, the genus was announced in Science in 2004.[1]

In late 2005, an experiment by Swedish marine biologists resulted in the discovery of a species of the worm in the North Sea off the west coast of Sweden. In the experiment, a minke whale carcass that had been washed ashore had been sunk to a depth of 120 m (390 ft) and monitored for several months. Biologists were surprised to find that, unlike the previous discoveries, the new species, colloquially known as "bone-eating snot flower" after its scientific name (Osedax mucofloris), lived in relatively shallow waters.

In November 2009, researchers reported finding as many as 15 species of boneworms living in Monterey Bay on the California coast.[17]

Sex determination

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Annelid sex is typically determined by genetic factors,[18] however models of environmental sex determination have been proposed for Osedax, in which larvae that settle on bones mature into females, while larvae that settle on female Osedax do not fully develop and mature into males.[19] O. japonicus in particular has showcased an environmental form of sex determination.[20]

Life cycle

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  • Mature female Osedax worms spawn eggs into the mucus attached to their tubes, where the embryos develop for 3 days.
  • Larvae then begin to swim in the water column. This is called the trochophore stage. The larvae settle on whale bones and begin crawling.
  • During the trocophore stage, male Osedax settle on the tubes of the females, where they are metamorphosed into dwarf males, which can be inside or outside the female tube.
  • 1 day after settling on bones, larvae use two pairs of chaetae to attach to the substrate. Juvenile worms begin to secrete mucus and develop two ventral palps on the dorsal side of the prostomium.
  • 2 days after settling, the palps elongate and the heart starts to beat. The roots attach to the bones begin to digest.
  • 4 days after settling, the trunk and ventral palps elongate, where symbiotic bacteria are detected in the root.
  • 7 days after settlement, pinnules extend from the ventral palps.
  • 10 days post settlement, the juvenile worms have 4 palps with pinnules, an oviduct, and a distinct root system.[21]

Symbiosis

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Symbionts are the primary providers of nutrition for Osedax.[22] However, these symbionts also possess genes, secretion systems, and toxins that disrupt the Osedax membrane and facilitate recurrent infections of adult Osedax through the root tips.[22][23] There is ongoing debate in the literature over whether the symbiosis in Osedax roots is commensal or mutualistic.[24][23] The symbiotic relationship between Osedax and its accompanying bacteria may be transferred either via vertical or horizontal transmission.[23]

Osedax species use collagen, which is the primary organic component in bone.[25] Collagen is degraded using a family of endopeptidases called matrix metalloproteinases (MMPs), which facilitates nutrient absorption by the Osedax.[25] The roots of the Osedax express high amounts of V-ATPase and carbonic anhydrase enzymes, which allows the Osedax to dissolve and absorb collagen and lipids.[25] Once dissolved, the nutrients are either used by the Osedax, or transported to the symbionts for further catabolism.[23][25]

As the endosymbionts lack secreted M9 peptidase, they rely on the Osedax worm to source extracellular collagen.[25] The symbionts in the Oceanospirillales order have then been observed to further process the collagen using collagenolytic enzymes.[23][26]

Sequencing of the Osedax worm genome has suggested an evolved dependency on its endosymbionts.[25] This is revealed by genomic streamlining, where increased functional groups were observed despite the loss of some gene families.[25] Six incomplete pathways were discovered in the Osedax worm genome which were supplemented by the endosymbionts.[25] In particular, the Osedax worm lacks specific gene families involved in bone lipid and carbohydrate metabolism.[25] This function is complemented by the Oceanospirillales symbionts, which utilize the glyoxylate cycle to catabolize nutrients from whale bones and convert fatty acids into carbohydrates.[25] The Osedax are then able to take up and store the end products as glycogen.[25] Bacteriocytes are present in the Osedax lower trunk subepidermal connective tissue,[25] and there are additional genes in the bacteriocytes that encode amino acids and glucose and aid in digestion and absorption of proteins into the roots.[27]

Endosymbionts

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The Oceanospirillales symbionts are found in the specialized roots[24] of all Osedax species,[28][23]  and play a major role in accelerating the degradation process of bones, as well as facilitating nutrient uptake for the Osedax.[24][25] Oceanospirillales are known for their ability to degrade complex organic compounds.[22][26]

Campylobacterales are abundant along the trunk of the Osedax according to a 2023 study.[24] Different genera in this order are found in Osedax at different points during the whale's degradation:

  1. Members of the Arcobacter genus are the primary early colonizers (<24 months).[24]
  2. Sulfurospirillum genus members colonize at ~50 months, during the transitional stages of organic carbon breakdown.[24]
  3. The Sulfurimonas genus dominates at >140 months, and are key players in its symbiosis with the Osedax host.[24]

The Sulfurimonas genus in particular protects the Osedax worms from potentially harmful by-products produced at >140 months of the whale fall degradation.[24] The Sulfurimonas bacteria house the type II and IV sulfide:quinone oxidoreductase genes that encode enzymes to oxidize and assimilate sulfide.[24] These reactions prevent the host from absorbing toxic by-products across the epithelial barrier.

Niche

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Osedax frankpressi

The role of Osedax in the degradation of marine vertebrate remains controversial. Some scientists[29] think that Osedax is a specialist on whalebones while others think that it is more of a generalist.[30][31] This controversy is due to a biogeographic paradox: despite the rarity and ephemeral nature of whale falls, Osedax has a broad biogeographic range and is surprisingly diverse.

One hypothesis advanced to explain this seeming paradox is that Osedax are able to colonize a variety of vertebrate remains besides whalebones. One study documented 14 new Osedax species successfully colonizing the bones of teleost fish, sea turtles, seals, cows, and turkeys, in addition to whales,[32] while a later study documented a new species feeding on the bones of alligators.[33] Osedax have also been observed colonizing terrestrial mammal bones mixed in with galley waste from a surface vessel. Other scientists[who?] have countered this hypothesis by pointing out how the cow bone experiment does not match any natural habitat and also the low probability of terrestrial mammal bones arriving at the ocean floor in significant quantities. They also point out other cases of food falls in which the remains disappeared too swiftly for Osedax colonization and the lack of any observed colonization in similar cases.[citation needed]

The true role of Osedax in the degradation of marine vertebrate remains is important to marine vertebrate taphonomy. Burrows closely similar to those made by Osedax species have been found in the bones of ancient marine birds and plesiosaurs, suggesting that the genus may once have had a wider range of foods.[34][35][36][37] In a study of the boring morphological diversity of Osedax, it was shown that the species difference of bone-boring is highly variable; within the same species, the boring morphology is only consistent in a particular bone, but not consistent in different bones. It was also suggested that multiple species of Osedax can co-exist in the same bone and in an incomplete spatial niche differentiation.[2]

The function of Osedax and their borings welcome other species such as Stephonyx amphipods, Paralomis crabs, and Rubyspira gastropods. As Osedax worms break down bone and lipid layers, fauna take advantage and colonize these bone matrices. Overall, the borings made by Osedax have shown to enhance biodiversity and the worms should, therefore, be considered ecosystem engineers. The downside of the deterioration caused by Osedax is that it speeds up the process of erosion, therefore only allowing this new fauna their new habitats for a temporary period.[38]

Evolution

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The oldest trace fossils on bones characteristic of Osedax are from a plesiosaur humerus from the Cambridge Greensand, England, likely reworked from late Albian (c. 100 million years old) sediments and a rib and costal plate from a sea turtle found in Cenomanian (100–93 million years ago) aged sediments of the Chalk Group, England. Osedax likely persisted on the bones of sea turtles after the extinction of most large marine reptiles at the end of the Cretaceous.[39] Osedax have the generalist ability to feed on different vertebrates (fishes, marine birds, whale bones).[40]

In terms of evolutionary history research, the Osedax could have had negative impact in preserving fossil record because its appearance at the shelf-depth combined with its ability to efficiently break down marine vertebrates skeletons.[39]

Species

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Osedax rubiplumus

Selected species:[41][32][42][43]

  • Osedax antarcticus Glover, Wiklund & Dahlgren, 2013
  • Osedax braziliensis Fujiwara, Jimi, Sumida, Kawato, Kitazato
  • Osedax bryani Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax craigmcclaini Berman, Hiley, Read, Rouse, 2024
  • Osedax crouchi Amon, Wiklund, Dahlgren, Copley, Smith, Jamieson & Glover, 2014
  • Osedax deceptionensis Taboada, Cristobo, Avila, Wiklund & Glover, 2013
  • Osedax docricketts Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax frankpressi Rouse, Goffredi & Vrijenhoek, 2004
  • Osedax jabba Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax japonicus Fujikura, Fujiwara & Kawato, 2006
  • Osedax knutei Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax lehmani Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax lonnyi Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax mucofloris Glover, Kallstrom, Smith & Dahlgren, 2005
  • Osedax nordenskjoeldi Amon, Wiklund, Dahlgren, Copley, Smith, Jamieson & Glover, 2014
  • Osedax priapus Rouse et al., 2014
  • Osedax packardorum Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax randyi Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax rogersi Amon, Wiklund, Dahlgren, Copley, Smith, Jamieson & Glover, 2014
  • Osedax roseus Rouse, Worsaae, Johnson, Jones & Vrijenhoek, 2008
  • Osedax rubiplumus Rouse, Goffredi & Vrijenhoek, 2004
  • Osedax ryderi Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax sigridae Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax talkovici Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax tiburon Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax ventana Rouse, Goffredi, Johnson & Vrijenhoek
  • Osedax westernflyer Rouse, Goffredi, Johnson & Vrijenhoek

References

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Further reading

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