Zombie Worm

''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. ''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 .

Anatomy and physiology

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

Digestive system

''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. ''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. 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 is secreted into the seawater.

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. 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.

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.

''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.

Sexual dimorphism

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. Male dwarfism prevents competition with female ''Osedax'' worms for food and space. Conditions that favour dwarfism in male Osedax are:

# Eliminates competition between male and female ''Osedax'' as resources are limited,
# Sessile lifestyle: attach to and rely on females for food,
# Decreases difficulty in finding a mate.

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.

Reproduction

Discoveries

Female ''Osedax'' worms have been observed spawning both in the wild and in laboratory aquaria. ''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. In the adult, the bacteria are localised in the root-like structures that grow into the whale bone. 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.

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

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 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.

Sex determination

Annelid sex is typically determined by genetic factors, 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. ''O. japonicus'' in particular has showcased an environmental form of sex determination.

Life cycle

* 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.

Symbiosis

Symbionts are the primary providers of nutrition for ''Osedax.'' 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. There is ongoing debate in the literature over whether the symbiosis in ''Osedax'' roots is commensal or mutualistic. The symbiotic relationship between ''Osedax'' and its accompanying bacteria may be transferred either via vertical or horizontal transmission.

''Osedax'' species use collagen, which is the primary organic component in bone. Collagen is degraded using a family of endopeptidases called matrix metalloproteinases (MMPs), which facilitates nutrient absorption by the ''Osedax''. 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. Once dissolved, the nutrients are either used by the ''Osedax'', or transported to the symbionts for further catabolism.

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

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

Endosymbionts

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

''Campylobacterales'' are abundant along the trunk of the ''Osedax'' according to a 2023 study. 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).
# ''Sulfurospirillum'' genus members colonize at ~50 months, during the transitional stages of organic carbon breakdown.
# The '' Sulfurimonas'' genus dominates at >140 months, and are key players in its symbiosis with the ''Osedax'' host.

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

Niche

The role of ''Osedax'' in the degradation of marine vertebrate remains controversial. Some scientists think that ''Osedax'' is a specialist on whalebones while others think that it is more of a generalist. 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, while a later study documented a new species feeding on the bones of alligators. ''Osedax'' have also been observed colonizing terrestrial mammal bones mixed in with galley waste from a surface vessel. Other scientists 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.

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.
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.

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.

Evolution

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. Further material is known from the Campanian and Maastrichtian. 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).

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.

Species

Selected species:Fujikura, Fujiwara & Kawato. ZOOLOGICAL SCIENCE 23: 733–740 (2006)
* '' 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

Further reading

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External links

Press release describing discovery of ''Osedax''

BBC website
– link to story about discovery of ''Osedax'' worms in the North Sea


* ttps://www.theguardian.com/environment/2022/aug/22/discovered-in-the-deep-the-worm-that-eats-bones-osedax Discovered in the deep: the worm that eats bones– The Guardian

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Sabellida