Osedax

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Osedax
Osedax frankpressi on a whale bone

Osedax frankpressi on a whale bone

Systematics
Class : Polychaete (Polychaeta)
Subclass : Palpata
Order : Canalipalpata
Subordination : Sabellida
Family : Beard worms (Siboglinidae)
Genre : Osedax
Scientific name
Osedax
Rouse et al., 2004

Osedax is a genus of beard worms (Siboglinidae) that specializes in colonizing skeletons on the ocean floor. The female worms live sessile on the bones of sunken dead animals and feed on nutrients in the bones via a kind of root system. They dissolve the bones through acid secretion and so release the nutrients from the mineral structure. Endosymbiotic bacteria, which live in a specialized tissue in the root system,playa role inthe digestion of fats and proteins from the bones. The microscopic males ( dwarf males ) are completely identical to the larval stage except for their sexual organs and live in large numbers in the living tubes of the females.

Was discovered Osedax in 2002. A scientist from the Monterey Bay Aquarium Research Institute examined with a diving robot ( ROV ) to deep-sea clams in Monterey Canyon , however, found by chance in three kilometers below the skeleton of a gray whale ( Eschrichtius robustus ). Its bones were densely populated by Osedax . 2004 took place then in Science the first description of the species by Greg W. Rouse, Shana K. Goffredi and the discoverer Robert C. Vrijenhoek . The name is borrowed from Latin and means "bone-eating".

morphology

Morphology of the female

Female of O. rubiplumus

The adult females a few centimeters long are typical of the genus . Its cylindrical trunk protrudes from the populated whale bone and lies in a transparent and gelatinous tube, which is secreted by glandular cells in the trunk epidermis . In addition to the glandular tissue, the trunk wall also contains longitudinal muscles with which the worm can retreat into its tube in case of danger. In the lower part of the trunk lies the heart, from which well-defined blood vessels emanate. As is typical for beard worms, adult Osedax do not have a mouth, intestinal tract or anus. Four little arms protrude from the tip of the trunk into the open water, finely feathered or smooth ( O. nude palp); the smooth arms of the so-called " O. nude palp" are only macroscopically smooth and show a lobed surface under the microscope. The little arms serve as gill-like respiratory organs and are usually reddish in color, but can also be greenish or almost white. The ends of the elongated fallopian tubes are located between these arms. They arise at the base of the hull and run along the hull in the tube until they protrude into the seawater between the gills. At its base, the trunk turns into a rounded thickening, the so-called ovisac . From this part on, the worm is embedded in its substrate bone. Root -like, greenish branches emanate from the ovisac and hollow out the bone. A striking exception to this physique is the still undescribed species Osedax spiral : the end of the trunk facing the water has no arms, but ends in a spiral. Your fallopian tubes do not protrude from the trunk.

The ovisac and the roots are surrounded on the outside by a single-layer epithelium , to which a thin and inconspicuous layer of muscle cells adjoins on the inside. A thick, green layer of tissue lies between these layers and a single-layer peritoneum that surrounds the coelom . It contains the bacteriocytes that harbor the Osedax endosymbiotic bacteria . The bacteria are partly free in the cell plasma , partly they are enclosed in vacuoles . The only other organelles of these cells are a nucleus and star-shaped structures of unknown function. In addition, bacteria-free cells with a strongly pronounced endoplasmic reticulum also exist in this tissue . Comparable tissues for housing endosymbiotic bacteria are known from all beard worms and are called trophosomes . However, it is unclear whether the various types of tissue harboring bacteria are homologous structures in the beard worms . In Osedax , the trophosome arises from the somatic part of the lateral mesoderm , in other beard worms it usually arises from a different region of the mesoderm and sometimes also from the endoderm .

Morphology of the male

The males of most Osedax species are extremely small at 0.2 to 1.1 millimeters. Their body organization corresponds to that of a recently settled trochophora larva, with a prostomium , a peristomium that is not clearly demarcated towards the rear and then a longer and a shorter body segment, without any recognizable pygidium . Numerous larval features are still present, such as the cilia ring called prototroch at the border of the prostomium and peristomium. There is no mouth opening or digestive tract, they feed on yolk for their lifetime. Spermatogonia lie ventrally at the front end of the unit of peristomium and the long segment combined as segment 1 . The spermatids they produce mature into sperm, which are carried by paired ciliary ligaments on the ventral side of the males' inner body wall into the vas deferens located behind the prostomium. The spermatic duct opens into the sac-like seminal vesicle in which the sperm are collected. The sexual opening of the males emerges from the seminal vesicle. The males do not inhabit endosymbiotic bacteria.

The males of O. priapus are an exception - they reach a third the body size of females of their kind and are organized in a similar way into a trunk protruding from the bone and a root system embedded in the bone. They can stretch their trunk, which is contracted in the resting state, to a multiple of its resting length, in order to inseminate neighboring females via a sexual pore at the tip of their trunk. In addition, like females, they have a trophosome with endosymbiotic bacteria. The ancestors of this species probably already had the dwarf males that are otherwise typical of the genus; their continued development in O. priapus thus represented an evolutionary reversal that only rarely occurs (see Dollosche's law ).

ecology

Skeleton of a gray whale ( Eschrichtius robustus ) at a depth of 1700 meters at the bottom of the Santa Cruz Basin. Also shown in the picture are hagfish

Osedax are marine life and colonize the bones of vertebrates that have sunk to the sea floor after their death. The food source for Osedax are the structural proteins (e.g. collagen ) and fats embedded in the mineral matrix (framework) of the bone . The animals have been found worldwide at sea depths of 20 meters to over 4 kilometers. The characteristic substrate for female Osedax worms is the bones of whales.

When a whale carcass sinks to the bottom of the sea, it represents an enormous nutrient impulse for the otherwise nutrient-poor soil regions of the deep sea . The substance of a whale forms the basis for an entire ecosystem that has a characteristic succession . Initially, mobile scavengers such as hagfish , sleeping sharks , grenadier fish and various invertebrates eat the soft tissue of the whale for months or even years. Once the skeleton is uncovered, opportunistic crustaceans and poly-bristles still exploit the remains on the bones and the organically enriched sediment around the whale. In whales, the bones themselves contain a lot of chemically bound energy, since they have been transformed into highly fatty cancellous bones for improved hydrostatic properties. The fats and collagens in the whale bones are exploited , among other things, by specialized, sulfate-breathing bacteria. In this phase characterized by exposed whale bones, Osedax worms colonize the skeleton of the whale, sometimes several species of Osedax at the same time. Whale skeletons colonized by a certain Osedax species can be completely colonized by another Osedax species after just a few months . In the Monterey Canyon, for example, the species O. rubiplumus is most frequently found on recently exposed whale ribs , which forms a flat and thread-like root system and thus particularly exploits the collagen-rich outer layers of the bone. On older skeletons, this species is then replaced by O. frankpressi , whose lobed and robust roots penetrate deeper into the bones and thus particularly exploit the spongy internal, fat-rich bone areas. In the later stages of this succession, the as yet undescribed taxonomic unit “O. spiral “ specializes in exploiting pieces of bone already covered by sediment with their roots. The different forms of the root system of coexisting Osedax species indicate a niche division , which could be an important factor for speciation in Osedax . Often, however, species with almost the same root morphology are also present on a skeleton, which tends to suggest a neutral theory .

Osedax does not specialize exclusively in whale bones, but also colonizes the bones of fish, other mammals, birds and, in rare cases, soft tissue from whales such as the spermaceti of sperm whales .

Reproduction and development

Osedax females are fertilized by the males who have settled in their gelatinous living tube. A few to over 100 of the microscopic males live in the living tubes of older females. The sperm of the males are individually floating and not released as spermatophores ; internal fertilization, which has not yet been further characterized, takes place. Sexually mature females colonized with males release an average of 335 fertilized eggs per day in the laboratory. Apparently, the eggs are given differently from species to species directly into the open water, or go through their early development in the female mucus. The egg cell goes through an uneven spiral furrow , and after one to three days a free-swimming trochophora has formed. This can actively swim and live on its yolk supplies for about two weeks. The larvae can then settle on bones, the first anchoring presumably taking place via two hook-shaped chaetae (bristles). They then begin to secrete the gelatinous living tube and develop adult traits in the female, such as the gill arms and the root system. Larger females are gradually colonized by small males until a large majority of males live in the population. As a possible basis for this population dynamics, an environmentally dependent sex determination is discussed at Osedax : If a larva settles on a bone, it develops into a female - on the other hand, it becomes a male if it settles on an adult female. There is as yet no clear evidence for this hypothesis.

physiology

Ingestion

The female absorbs nutrients from the bones via the root system, which is supplied with blood vessels right up to the tips. The epithelial cells of the roots, which are in contact with the environment, show many surface- enlarging microvilli , as are typical for substance-exchanging epithelia, as well as a strikingly high density of mitochondria . The digestion of proteins and lipids from the inorganic bone matrix used in the epithelial membrane embedded H + - ATPases under ATP -consumption protons (H + pumps from the epithelial cells). The H + pumped from the epithelial cells acidify the bone environment and consequently dissolve the mineral bone structure made of calcium phosphates such as hydroxyapatite . The proteins and fats now exposed are then absorbed through the membrane of the root epithelium. A constant supply of protons for this process provides carbonic acid (H 2 CO 3 , dissociates to H + + HCO 3 - ), which is created from a reaction of water with carbon dioxide. The formation of carbonic acid from water and carbon dioxide is promoted by a carbonic anhydrase , which the worms' root tissue produces in large quantities.

This bone dissolution procedure requires the constant formation of new carbon dioxide. The carbon dioxide required for this comes from the oxygen-consuming cell respiration - the immediate vicinity of the bones and thus also the roots, however, is extremely low in oxygen (anoxic) due to bacterial activities. In order to supply their own metabolism and that of the endosymbiotic bacteria with sufficient oxygen, the Osedax females have very efficient respiratory organs with their gill arms protruding far beyond the substrate bones. Excess HCO 3 - is probably also disposed of via these gills , in order to remove it from the reaction equilibrium of carbonic acid formation and to promote the formation of new H 2 CO 3 . Sulphate-consuming bacteria also produce high concentrations of highly toxic hydrogen sulphide in the bone environment; It is still unknown which physiological mechanism allows Osedax to tolerate these high concentrations.

Endosymbiosis

The proteins and fats absorbed by the roots from the colonized bones serve Osedax as a source of energy and organic compounds. Γ-proteobacteria from the order of the Oceanospirillales play an important role in the metabolism and nutrition of worms . Strains of this bacterial group are always found in adult females by Osedax and are in a symbiotic relationship with the worms, which supports the worm in its metabolism and nutrition. In some species of Osedax , representatives of the ε-proteobacteria were also found as endosymbionts. The bacteria are not passed on from the parent animals to the young animals, but are taken up again from the environment by each individual. An individual can acquire various bacterial strains as endosymbionts from several opportunistic infections. Individual bacterial strains do not appear to be specifically bound to certain Osedax species. Genetic findings on two strains of Oceanospirillales endosymbiotic at Osedax speak for a presumed free-living stage of the symbiotic bacteria : They have genes for the formation of flagella as well as for receptors for the recognition of extracellular molecules, which are in a free stage of movement and the locating of Osedax hosts could serve. The symbiosis is not yet fully understood; Beard worms often enter into symbiosis with bacteria, but these are usually chemoautotrophic bacteria that are able to fix free carbon. The Osedax symbionts are heterotrophic , which is unique to beard worms. This means that the worm must first supply its symbionts with energy and precursor molecules before it can benefit from the bacteria 's metabolism.

A role of bacteria in the fatty acid metabolism of the worm can be seen in the abundance of cis - vaccenic acid and eicosapentaenoic acid in their tissues. The former is a typical end product of microbial fatty acid metabolism, the latter is known as a membrane component of some Oceanospirillales deep-sea microbes, as it contributes to the maintenance of biomembrane fluidity under high pressure and at low temperatures . The worm gets at least part of its fatty acids from the metabolism of the γ-proteobacteria. Wax esters , whose bound fatty acids are very likely to be cis -vaccenic acids , serve Osedax as storage substances. Contrary to previous assumptions, the symbionts do not have a collagen-dissolving (collagenolytic) function, since there are no genes for collagenases in their genomes . This structural protein of the bones is presumably first split into oligopeptides and amino acids by the worm before it reaches the bacteria. Genome analyzes of symbiont strains showed the ability of these bacteria to re-synthesize all B vitamins , including vitamin B 12 , which is essential for all animals , as well as to re-synthesize 18 of the 20 natural amino acids. They also have genes that code for export proteins for various essential amino acids. As part of the symbiosis, the bacteria receive the fats, proteins and other molecules released from the bone by the worm. In return, the worm receives fatty acids as well as essential amino acids and vitamins from the metabolism of the bacteria.

Bacteriocytes that are active in dividing with intact symbionts are particularly present in the root tissue, while in bacteriocytes in the direction of the ovisac there is increasing digestion of symbionts within vacuoles. In addition, the frequency of apoptotic bacteriocytes increases in the ovisac area . A certain life cycle of bacteriocytes and endosymbionts is therefore assumed, which begins in the actively dividing tissue of the roots and ends with digestion of the bacteria and apoptosis of the bacteriocytes after migration towards the ovisac .

Systematics

Relationships of the Siboglinidae
 Siboglinidae 

Frenulata


   

Osedax


   

Sclerolinum


   

Vestimentifera





Template: Klade / Maintenance / Style

Morphological characteristics and DNA analyzes show Osedax to belong to the family of beard worms (Siboglinidae). Sister group of Osedax is a clade from Vestimentifera (a large group of beard worms) and its sister group, the so far hardly explored genus Sclerolinum . Osedax and the clade from Vestimentifera and Sclerolinum form the sister group to the other large group of beard worms, the Frenulata . The type species of Osedax is O. rubiplumus . In the meantime, 25 species of Osedax have been described with a scientific name worldwide :

In addition, however, numerous other species are known whose scientific description and naming are still pending. In scientific discourse, they are referred to as operational taxonomic units (OTUs) and are given working names based on their appearance.

evolution

Tribal history

Osedax is a genus very old genus. In 2015, cavities were found in a 100-million-year-old bone of a plesiosaur , the shape of which corresponds to the bone cavities created by today's Osedax : A short cylindrical opening is followed by an irregularly shaped cavity created by the root system. This so far oldest find of Osedax traces indicates that the evolution of Osedax was chronologically connected to the emergence of large Mesozoic marine reptiles. Their skeletons served the early Osedax worms as food. Also Cretaceous traces of Osedax were on fossil bones of sea turtles found. These findings move the previously assumed young evolutionary age of the beard worms by many millions of years back to the Mesozoic. After the extinction of the large marine reptiles at the KT border , Osedax survived thanks to the highly specialized diet that allows them to colonize the bones of smaller marine animals. This included sea turtles on the one hand, and Oligocene Osedax holes in fossils of early seabirds of the Plotopteridae family and in fossilized fish bones on the other . With the appearance of the whales, Osedax opened up a new and probably the most important source of food today with their skeletons, as boreholes in Oligocene and Pliocene whale fossils show. Some paleontologists suspect that Osedax may have significantly impaired the fossil preservation of marine vertebrates by consuming bones. The so-called " Osedax effect" must be taken into account when evaluating the fossil record of many vertebrate groups.

Male dwarfing

The evolution of dwarf males is often promoted by a scarcity of resources, difficult partner searches, a sessile lifestyle and little competition between males for females. With a way of life in the deep sea on only sporadic skeletons, these factors applied to Osedax and promoted the evolution of a distinctive sex dimorphism . Here, those females have a higher evolutionary fitness who grow quickly on the scarce resources (bones) and can exploit them efficiently and thus achieve higher fertility. In males, on the other hand, early sexual maturity and high mobility are advantageous - this increases the probability of reaching one of the widely scattered habitat islands and fertilizing a female. This selection pressure led the males to sexual maturity in the larval stage. In this way, competition for limited resources between females and males has also been eliminated. The relapse in O. priapus to larger males is still unexplained, but even in this species the males only reach a third of the body size of females. Sexual selection could have promoted the emergence of larger males, as such a male with an extendible trunk has access to several females and can thus produce more offspring than a dwarf male, which is confined to the living tube of a single female. Too little is known about the biology of this species to be able to make well-founded statements.

supporting documents

  1. ↑ Archive link ( Memento of the original from October 1, 2015 in the Internet Archive ) Info: The archive link was inserted automatically and has not yet been checked. Please check the original and archive link according to the instructions and then remove this notice. , accessed September 6, 2015  @1@ 2Template: Webachiv / IABot / www.mbari.org
  2. ↑ a b c d e f g h Rouse, Greg W .; Shana K. Goffredi, Robert C. Vrijenhoek (2004): Osedax: Bone-Eating Marine Worms with Dwarf Males . Science 305 (5684), pp. 668-671. doi : 10.1126 / science.1098650
  3. ↑ a b c d Amon, Diva J .; Helena Wiklund, Thomas G. Dahlgren, Jonathan T. Copley, Craig R. Smith, Alan J. Jamieson, Adrian G. Glover (2014): Molecular taxonomy of Osedax (Annelida: Siboglinidae) in the Southern Ocean . Zoologie Script 43 (4), pp. 405-417.
  4. ↑ a b Vrijenhoek, Robert C .; Shannon B. Johnson, Greg W. Rouse (2009): A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida) . BMC Biology 7, p. 74.
  5. ↑ a b Katz, Sigrid; Waltraud Klepal, Monika Bright (2011): The Osedax Trophosome: Organization and Ultrastructure . The Biological Bulletin 220, pp. 128-139.
  6. ↑ Eichinger, Irmgard; Waltraud Klepal, Markus Schmid, Monika Bright (2011): Organization and Microanatomy of the Sclerolinum contortum Trophosome (Polychaeta, Siboglinidae) . The Biological Bulletin 220, pp. 140-153.
  7. ↑ Worsaae, Katrine; Greg W. Rouse (2010): The simplicity of males: Dwarf males of four species of Osedax (Siboglinidae; Annelida) investigated by confocal laser scanning microscopy . Journal of Morphology 271, pp. 127-142.
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  25. ↑ a b Tresguerres, Martin; Sigrid Katz, Greg W. Rouse (2013): How to get into bones: proton pump and carbonic anhydrase in Osedax boneworms . Proceedings of the Royal Society B 280, p. 20130625.
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  27. ↑ a b Goffredi, Shana K .; Shannon B. Johnson, Robert C. Vrijenhoek (2007): Genetic Diversity and Potential Function of Microbial Symbionts Associated with Newly Discovered Species of Osedax Polychaete Worms . Applied and Environmental Microbiology 73 (7), pp. 2314-223.
  28. ↑ Verna, Caroline; Alban Ramette, Helena Wiklund, Thomas G. Dahlgren, Adrian G. Glover, Françoise Gaill, Nicole Dubliere (2010): High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic . Environmental Microbiology 12 (8), pp. 2355-2370.
  29. ↑ a b c Goffredi, Shana K .; Hana Yi, Qingpeng Zhang, Jane E. Klann, Isabelle A. Struve, Robert C. Vrijenhoek, Titus Brown (2014): Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms . ISME Journal 8 (4), pp. 908-924.
  30. ↑ Goffredi, Shana K .; Victoria J. Orphan, Greg W. Rouse, Linda Jahnke, Tsegeria Embaye, Kendra Turk, Ray Lee, Robert C. Vrijenhoek (2005): Evolutionary innovation: a bone-eating marine symbiosis . Environmental Microbiology 7 (9), pp. 1369-1378.
  31. ↑ a b c d e f g h i j k l m n Greg W. Rouse, Shana K. Goffredi, Shannon B. Johnson and Robert C. Vrijenhoek. 2018. An Inordinate Fondness for Osedax (Siboglinidae: Annelida): Fourteen New Species of Bone Worms from California. Zootaxa . 4377 (4); 451-489. DOI: 10.11646 / zootaxa.4377.4.1
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  33. ↑ Schander, Christoffer; Hans Tore Rapp, Thomas G. Dahlgren (2010): Osedax mucofloris (Polychaeta, Siboglinidae), a bone-eating marine worm new to Norway . Fauna norvegica 30, pp. 5-8.
  34. ↑ a b c Danise, Silvia; Nicholas D. Higgs (2015): Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls . Biology Letters 11 (4): 20150072.
  35. ↑ Kiel, Steffen; Wolf-Achim Kahl, James L. Goedert (2011): Osedax borings in fossil marine bird bone . Natural Sciences 98 (1), pp. 51-55.
  36. ↑ Kiel, Steffen; Wolf-Achim Kahl, James L. Goedert (2013): Traces of the bone-eating annelid Osedax in Oligocene whale teeth and fish bones . Palaeontological Journal 87 (1), pp. 161–167.
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  38. ↑ Higgs, Nicholas D .; Crispin TS Little, Adrian G. Glover, Thomas G. Dahlgren, Craig R. Smith, Stefano Dominici (2012): Evidence of Osedax worm borings in Pliocene (∼3 Ma) whale bone from the Mediterranean . Historical Biology 24 (3), pp. 269-277.
  39. ↑ Vrijenhoek, Robert C .; Shannon B. Johnson, Greg W. Rouse (2008): Bone-eating Osedax females and their 'harems' of dwarf males are recruited from a common larval pool . Molecular Ecology 17, pp. 4535-4544.

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This article was added to the list of excellent articles on November 22, 2015 in this version .