Osedax is a
genus of deep-sea
siboglinidpolychaetes, 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.
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 (1 to 3 inches), although this varies between species (cite).[4] Sexual dimorphism is observed in Osedax with females >20,000 times larger than males.[5]
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.[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
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 and produce sperm.[5] Male dwarfism prevents competition with female Osedax worms for food and space.[5] Conditions that favour dwarfism in male Osedax are:
Eliminates competition between male and female Osedax as resources are limited,[11]
Sessile lifestyle: attach to and rely on females for food,[11]
Interestingly, Osedax priapus lack the frequently observed sexual size dimorphism, and males have similar size to females. This results in competition for space and food.[5] These male worms are able to produce more sperm. However, sexual size dimorphism is still observed in O. priapus where 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.[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
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
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
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
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:
Members of the Arcobacter genus are the primary early colonizers (<24 months).[24]
Sulfurospirillum genus members colonize at ~50 months, during the transitional stages of organic carbon breakdown.[24]
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
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 paradox is that Osedax are able to colonize a variety of vertebrate remains besides whalebones. This hypothesis is supported by an experiment involving cow bones suspended above the sea floor. A variety of Osedax species successfully colonized these bones. 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.[32][33][34] 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.[35]
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.2 100 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.[36]Osedax have the generalist ability to feed on different vertebrates (fishes, marine birds, whale bones).[37]
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.[36]
^
abG. W. Rouse; N. G. Wilson; S. K. Goffredi; S. B. Johnson; T. Smart; C. Widmer; C. M. Young & R. C. Vrijenhoek (2009). "Spawning and development in Osedax boneworms (Siboglinidae, Annelida)". Marine Biology. 156 (3): 395–405.
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^Piper, Ross (2007), Extraordinary Animals: An Encyclopedia of Curious and Unusual Animals,
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^Kaplan, Matt (2010). "Bone-boring worm once had a taste for birds. Osedax worms might have had a more-rounded diet 30 million years ago". Nature.
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10.1038/news.2010.651.