Osedax

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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.<ref name=":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 Template:Convert.

Anatomy and physiologyEdit

Osedax are colorful tubeworms that have no mouth, anus, or gut.<ref name=":4">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> The body is divided into different regions: trunk, ovisac, and root. They range in length between Template:Convert, although this varies between species (cite).<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> Sexual dimorphism is observed in Osedax with females >20,000 times larger than males.<ref name=":5">Template:Cite journal</ref>

Digestive systemEdit

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.<ref>Template:Cite news</ref> 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.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> 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 HCOTemplate:Subsup is secreted into the seawater.<ref name=":1">Template:Cite journal</ref>

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.<ref name=":0">Template:Cite journal</ref> 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.<ref name=":0" />

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.<ref>Template:Cite journal</ref>

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.<ref name=":1" />

Sexual dimorphismEdit

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.<ref name=":5" /> Male dwarfism prevents competition with female Osedax worms for food and space.<ref name=":5" /> Conditions that favour dwarfism in male Osedax are:

Eliminates competition between male and female Osedax as resources are limited,<ref name=":6">Template:Cite journal</ref>
Sessile lifestyle: attach to and rely on females for food,<ref name=":6" />
Decreases difficulty in finding a mate.<ref name=":6" />

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.<ref name=":5" />

ReproductionEdit

DiscoveriesEdit

Female Osedax worms have been observed spawning both in the wild and in laboratory aquaria.<ref name=":7" /> 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.<ref name=":7">Template:Cite journal</ref> In the adult, the bacteria are localised in the root-like structures that grow into the whale bone.<ref>Template:Cite journal</ref><ref>Piper, Ross (2007), Extraordinary Animals: An Encyclopedia of Curious and Unusual Animals, Greenwood Press.</ref> 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.<ref>Template:Cite journal</ref><ref>Template:Cite journal</ref>

Following its discovery in 2002 by researchers at the Monterey Bay Aquarium Research Institute, the genus was announced in Science in 2004.<ref name=RG&V/>

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 Template:Convert 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.<ref>Template:Cite journal</ref>

Sex determinationEdit

Annelid sex is typically determined by genetic factors,<ref>Template:Cite journal</ref> 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.<ref>Template:Cite journal</ref> O. japonicus in particular has showcased an environmental form of sex determination.<ref>Template:Cite journal</ref>

Life cycleEdit

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.<ref>Template:Cite journal</ref>

SymbiosisEdit

Symbionts are the primary providers of nutrition for Osedax.<ref name=":8">Template:Cite journal</ref> 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.<ref name=":8" /><ref name=":9">Template:Cite journal</ref> There is ongoing debate in the literature over whether the symbiosis in Osedax roots is commensal or mutualistic.<ref name=":10">Template:Cite journal</ref><ref name=":9" /> The symbiotic relationship between Osedax and its accompanying bacteria may be transferred either via vertical or horizontal transmission.<ref name=":9" />

Osedax species use collagen, which is the primary organic component in bone.<ref name=":11">Template:Cite journal</ref> Collagen is degraded using a family of endopeptidases called matrix metalloproteinases (MMPs), which facilitates nutrient absorption by the Osedax.<ref name=":11" /> 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.<ref name=":11" /> Once dissolved, the nutrients are either used by the Osedax, or transported to the symbionts for further catabolism.<ref name=":9" /><ref name=":11" />

As the endosymbionts lack secreted M9 peptidase, they rely on the Osedax worm to source extracellular collagen.<ref name=":11" /> The symbionts in the Oceanospirillales order have then been observed to further process the collagen using collagenolytic enzymes.<ref name=":9" /><ref name=":12">Template:Cite journal</ref>

Sequencing of the Osedax worm genome has suggested an evolved dependency on its endosymbionts.<ref name=":11" /> This is revealed by genomic streamlining, where increased functional groups were observed despite the loss of some gene families.<ref name=":11" /> Six incomplete pathways were discovered in the Osedax worm genome which were supplemented by the endosymbionts.<ref name=":11" /> In particular, the Osedax worm lacks specific gene families involved in bone lipid and carbohydrate metabolism.<ref name=":11" /> 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.<ref name=":11" /> The Osedax are then able to take up and store the end products as glycogen.<ref name=":11" /> Bacteriocytes are present in the Osedax lower trunk subepidermal connective tissue,<ref name=":11" /> 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.<ref>Template:Cite journal</ref>

EndosymbiontsEdit

The Oceanospirillales symbionts are found in the specialized roots<ref name=":10" /> of all Osedax species,<ref>Template:Cite journal</ref><ref name=":9" /> and play a major role in accelerating the degradation process of bones, as well as facilitating nutrient uptake for the Osedax.<ref name=":10" /><ref name=":11" /> Oceanospirillales are known for their ability to degrade complex organic compounds.<ref name=":8" /><ref name=":12" />

Campylobacterales are abundant along the trunk of the Osedax according to a 2023 study.<ref name=":10" /> Different genera in this order are found in Osedax at different points during the whale's degradation:

Members of the Arcobacter genus are the primary early colonizers (<24 months).<ref name=":10" />
Sulfurospirillum genus members colonize at ~50 months, during the transitional stages of organic carbon breakdown.<ref name=":10" />
The Sulfurimonas genus dominates at >140 months, and are key players in its symbiosis with the Osedax host.<ref name=":10" />

The Sulfurimonas genus in particular protects the Osedax worms from potentially harmful by-products produced at >140 months of the whale fall degradation.<ref name=":10" /> The Sulfurimonas bacteria house the type II and IV sulfide:quinone oxidoreductase genes that encode enzymes to oxidize and assimilate sulfide.<ref name=":10" /> These reactions prevent the host from absorbing toxic by-products across the epithelial barrier.

NicheEdit

File:Osedax frankpressi.jpg

Osedax frankpressi

The role of Osedax in the degradation of marine vertebrate remains controversial. Some scientists<ref>Glover et al. 2005; Dahlgren et al. 2006; Fujijura et al. 2006</ref> think that Osedax is a specialist on whalebones while others think that it is more of a generalist.<ref>Jones et al. 2008</ref><ref>Template:Cite journal</ref> 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,<ref name=":13" /> while a later study documented a new species feeding on the bones of alligators.<ref>Template:Cite journal</ref> Osedax have also been observed colonizing terrestrial mammal bones mixed in with galley waste from a surface vessel. Other scientistsTemplate: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.Template: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. <ref name="JamisonToddetal2020">Template:Cite journal</ref><ref>Template:Cite journal</ref><ref>Template:Cite journal</ref><ref>Template:Cite news</ref> 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.<ref name=":2">Template:Cite journal</ref>

The presence 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.<ref>Template:Cite journal</ref>

EvolutionEdit

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.<ref name=":3">Template:Cite journal</ref> Further material is known from the Campanian and Maastrichtian.<ref name="JamisonToddetal2020"/> Following the extinction of almost all large marine reptiles at the end of the Cretaceous, Osedax likely persisted on the bones of sea turtles and fish. Given that Osedax have the generalist ability to feed on different vertebrates (fishes, marine birds, whale bones).<ref>Template:Cite journal</ref>

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.<ref name=":3" />

SpeciesEdit

File:Osedax rubiplumus.jpg

Osedax rubiplumus

Selected species:<ref>WoRMS, Genus Osedax</ref><ref name=":13">Template:Cite journal</ref><ref>Template:Cite journal</ref><ref>Fujikura, Fujiwara & Kawato. ZOOLOGICAL SCIENCE 23: 733–740 (2006)</ref>

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