Trophosome

Last updated

A trophosome is a highly vascularised organ found in some animals that houses symbiotic bacteria that provide food for their host. Trophosomes are contained by the coelom of the vestimentiferan tube worms (Siboglinidae, e.g. the giant tube worm Riftia pachyptila ) [1] and in the body of symbiotic flatworms of the genus Paracatenula . [2]

Contents

The trophosome of Riftia pachyptila. The Giant Tube Worm, Riftia pachyptila and its Trophosome.png
The trophosome of Riftia pachyptila .

Organization

Initially, the trophosome in frenulates and vestimentiferans had been identified as a mesodermal tissue. [4] The discovery of bacteria inside the trophosomal tissue only occurred in 1981 when the ultrastructure of trophosome of several frenulate species and of Sclerolinum brattstromi was studied. [5] The bacteriocytes and symbionts composed of 70.5% and 24.1% of the trophosome's volume respectively. [1] Generally, trophosome extends over the entire trunk region between the two longitudinal blood vessels from immediately posterior to the ventral ciliary band of the forepart to the posterior end of the trunk delineated by the septum between trunk and first opisthosomal segment. [4] The trophosome can be differentiated between anterior and a posterior area due to incremental changes in host tissue organization, the amount of bacteriocytes, the size and shape of symbionts. [4] The trophosome consisted anteriorly of a small number of bacteriocytes and extensive mesenchyma, while the posterior of trophosome subsequently consisted of a large population of bacteriocytes and a peripheral peritoneum. [4]

Bacteriocytes and symbionts

The bacteriocyte cytoplasm is abundant in glycogen and contains some electron-dense, round-shape granules. [4] Mitochondria and the rough endoplastic reticulum are low in number. Throughout the anterior trophosome region, the nuclei were mainly oval but irregularity in the shape of the nuclei is observed in the posterior trophosome region. [4] The cell wall of the symbionts composed of an outer membrane and a cytoplasmic membrane typical of gram-negative bacteria. [6] Symbionts were often embedded separately in the symbiosome membrane adjacent to the bacterial cell wall except when they are proliferating. [4] In such case, proliferating symbionts are frequently found in the anterior trophosome region.

Structural organization

(A) Squeeze preparation of a live Paracatenula galateia specimen under incident light showing the smooth, silky appearance of the trophosome and the transparent rostrum. (B) TEM trophosome region cross section. One bacteriocyte (surrounded by a dashed line), the thin epidermis, neoblast stem cells and dorso-ventral muscles are labeled. The Ultrastructure of the Trophosome Region.png
(A) Squeeze preparation of a live Paracatenula galateia specimen under incident light showing the smooth, silky appearance of the trophosome and the transparent rostrum. (B) TEM trophosome region cross section. One bacteriocyte (surrounded by a dashed line), the thin epidermis, neoblast stem cells and dorso-ventral muscles are labeled.

In frenulates

In frenulates, the trophosome is limited to the post-annular portion of the trunk. [4] While a structural variant of the frenulate trophosome seems to occur, this organ typically consists of two epithelium and blood spaces sandwiched between the basal matrix of the epithelia in which the inner one is composed of bacteriocytes and the outer one is the coelomic lining. [4] The trophosome of Sclerolinum brattstromi consists of a centre of bacteriocytes surrounded by blood space and epithelium. [4]

In vestimentiferans

The trophosome of vestimentiferans is a complex, multi-lobed body with a vascular blood system that covers the entire trunk region. [1] Each lobule consists of a tissue of bacteriocytes enclosed by an aposymbiotic coelothel. It is traversed by an axial efferent blood vessel, and is supplied with ramifying peripheral afferent blood vessels. [4]

In Osedax

In Osedax , only the female has the trophosome. The trophosome in Osedax is made up of non symbiotic bacteria that reside between the muscle layer of the body's wall and the peritoneum in the ovisac and root regions; therefore, it is derived from the somatic mesoderm. [8] [4]

Trophosome color

The host lacks entirely a digestive system but derives all the essential nutrients from its endosymbiont . The host in turn provides the endosymbiont with all necessary inorganic compounds for chemolithoautotrophy. Inorganic elements, such as hydrogen sulphide, are oxidized by bacteria to produce energy for carbon fixation. [5] Trophosome tissue containing large quantities of concentrated sulphur has a light yellowish color. During sulfur limitation, i.e. when energy supply is reduced due to low concentrations of environmental sulfur, the stored sulfur is absorbed and the trophosome appears much darker. [9] [10] [11] Therefore, the energetic state of the symbiosis can be specifically interpreted from the color of the trophosome.

Trophosome growth

Trophosome tissue development happens by stem cells in the center of each lobule, contributing to new lobules as well as the regeneration of bacteriocytes circulating from the center to the periphery of each lobule through which apoptosis happens. [12] The trophosome tissue thus not only shows high levels of proliferation but also fairly small levels of apoptosis. Furthermore, symbionts in the periphery are constantly digested and replaced by separating symbionts in the middle. [13]

Lysophosphatidylethanolamines and free fatty acids are the products of phospholipid hydrolysis by phospholipases through the normal degradation of the membranes. [14] The presence of fairly high levels of lysophosphatidylethanolamines and fatty acids in trophosome indicate the high turnover of host and symbiont cells in the trophosome contributing to tissue and membrane degradation. [12]

Chemolithoautotrophy

In both these animals, the symbiotic bacteria that live in the trophosome oxidize sulfur or sulfide found in the worm's environment and produce organic molecules by carbon dioxide fixation that the hosts can use for nutrition and as an energy source. This process is known as chemosynthesis or chemolithoautotrophy.

Carbon transfer

Two different modes of carbon transfer from the symbionts to the host have been suggested.

Carbon fixation

Trophosome observed high activity of ribulose-1,5-bisphosphate carboxylase / oxygenase and ribulose 5-phosphate kinase, the enzymes of the Calvin-Benson CO2 fixation cycle. [16] It is important to notice that the observed activities of two enzymes, ribulose-1,5-bisphosphate carboxylase / oxygenase and ribulose 5-phosphate kinase, are present at high concentrations in the trophosome, but are absent in the muscle. [17] Furthermore, rhodanese, APSreductase, and ATP-sulfurylase are involved in adenosine triphosphate synthesis using the energy found in sulfur compounds such as hydrogen sulphide. These findings contribute to the conclusion that the symbiont of R. pachyptila is capable of producing ATP by means of sulfide oxidation, and that ATP energy could be used to fix carbon dioxide.

Glycogen storage in trophosome

In Riftia pachyptila , the glycogen content of 100 μmol glycosyl units g−1 fresh wt determined in the trophosome is divided equally between host and symbionts. [18] Although the symbionts take up only 25% of the trophosome, glycogen content is distributed equally between both partners, and this ratio remains similar for up to 40 h of hypoxia. Thus, host and symbiont each contain about 50 μmol glycosyl units g−1 fresh wt of trophosome. This amount is comparable to that in other host tissues of R. pachyptila, e.g. in the body wall (35 μmol glycosyl units g−1 fresh wt) or the vestimentum (20 μmol glycosyl units g−1 fresh wt), to that of other chemoautotrophic symbiotic animals and to that of nonsymbiotic animals known to be adapted to long-term anoxic periods. [19]

Host-microbe interaction

Protection against oxidative damage

Higher concentration of oxygen in the trophosome, (partial) anaerobic metabolism of the host, and host ROS-detoxifying enzymes in this tissue will not only shield the symbionts from oxidative damage but also minimize competition between the host and its oxygen symbionts. [20]

Symbiont population control

Symbiont population control can be largely the result of symbiont digestion, which essentially prevents symbionts from escaping from their compartments and/or overgrowing the host. [20] Nevertheless, the immune system can incorporate in phage defence and symbiont recognition during symbiosis. [20]

Communication between host and microbe

The host communication may be involving the eukaryote-like protein structure. [20] These symbiont proteins which number more than 100 in the trophosome samples suggest a symbiotic-relevant role. [20] Ankyrin repeats were believed to assist in the protein-protein interactions. [21] The ankyrin repeat proteins could interact directly with the host proteins in order to modulate endosome maturation and interfere with host symbiont digestion. [20]

See also

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

<span class="mw-page-title-main">Siboglinidae</span> Family of annelid worms

Siboglinidae is a family of polychaete annelid worms whose members made up the former phyla Pogonophora and Vestimentifera. The family is composed of around 100 species of vermiform creatures which live in thin tubes buried in sediment (Pogonophora) or in tubes attached to hard substratum (Vestimentifera) at ocean depths ranging from 100 to 10,000 m. They can also be found in association with hydrothermal vents, methane seeps, sunken plant material, and whale carcasses.

<span class="mw-page-title-main">Marine worm</span>

Any worm that lives in a marine environment is considered a water worm. Marine worms are found in several different phyla, including the Platyhelminthes, Nematoda, Annelida, Chaetognatha, Hemichordata, and Phoronida. For a list of marine animals that have been called "sea worms", see sea worm.

<span class="mw-page-title-main">Chemosynthesis</span> Biological process building organic matter using inorganic compounds as the energy source

In biochemistry, chemosynthesis is the biological conversion of one or more carbon-containing molecules and nutrients into organic matter using the oxidation of inorganic compounds or ferrous ions as a source of energy, rather than sunlight, as in photosynthesis. Chemoautotrophs, organisms that obtain carbon from carbon dioxide through chemosynthesis, are phylogenetically diverse. Groups that include conspicuous or biogeochemically important taxa include the sulfur-oxidizing Gammaproteobacteria, the Campylobacterota, the Aquificota, the methanogenic archaea, and the neutrophilic iron-oxidizing bacteria.

<i>Riftia</i> Giant tube worm (species of annelid)

Riftia pachyptila, commonly known as the giant tube worm and less commonly known as the giant beardworm, is a marine invertebrate in the phylum Annelida related to tube worms commonly found in the intertidal and pelagic zones. R. pachyptila lives on the floor of the Pacific Ocean near hydrothermal vents. The vents provide a natural ambient temperature in their environment ranging from 2 to 30 °C, and this organism can tolerate extremely high hydrogen sulfide levels. These worms can reach a length of 3 m, and their tubular bodies have a diameter of 4 cm (1.6 in).

Horizontal transmission is the transmission of organisms between biotic and/or abiotic members of an ecosystem that are not in a parent-progeny relationship. This concept has been generalized to include transmissions of infectious agents, symbionts, and cultural traits between humans.

<i>Lamellibrachia</i> Genus of annelids

Lamellibrachia is a genus of tube worms related to the giant tube worm, Riftia pachyptila. They live at deep-sea cold seeps where hydrocarbons leak out of the seafloor, and are entirely reliant on internal, sulfide-oxidizing bacterial symbionts for their nutrition. The symbionts, gammaproteobacteria, require sulfide and inorganic carbon. The tube worms extract dissolved oxygen and hydrogen sulfide from the sea water with the crown of plumes. Species living near seeps can also obtain sulfide through their "roots", posterior extensions of their body and tube. Several sorts of hemoglobin are present in the blood and coelomic fluid to bind to the different components and transport them to the symbionts.

<span class="mw-page-title-main">Gammaproteobacteria</span> Class of bacteria

Gammaproteobacteria is a class of bacteria in the phylum Pseudomonadota. It contains about 250 genera, which makes it the most genus-rich taxon of the Prokaryotes. Several medically, ecologically, and scientifically important groups of bacteria belong to this class. It is composed by all Gram-negative microbes and is the most phylogenetically and physiologically diverse class of Proteobacteria.

<span class="mw-page-title-main">Colleen Cavanaugh</span> American microbiologist

Colleen Marie Cavanaugh is an American academic microbiologist best known for her studies of hydrothermal vent ecosystems. As of 2002, she is the Edward C. Jeffrey Professor of Biology in the Department of Organismic and Evolutionary Biology at Harvard University and is affiliated with the Marine Biological Laboratory and the Woods Hole Oceanographic Institution. Cavanaugh was the first to propose that the deep-sea giant tube worm, Riftia pachyptila, obtains its food from bacteria living within its cells, an insight which she had as a graduate student at Harvard. Significantly, she made the connection that these chemoautotrophic bacteria were able to play this role through their use of chemosynthesis, the biological oxidation of inorganic compounds to synthesize organic matter from very simple carbon-containing molecules, thus allowing organisms such as the bacteria to exist in deep ocean without sunlight.

<i>Lamellibrachia luymesi</i> Species of tube worms in the family Siboglinidae

Lamellibrachia luymesi is a species of tube worms in the family Siboglinidae. It lives at deep-sea cold seeps where hydrocarbons are leaking out of the seafloor. It is entirely reliant on internal, sulfide-oxidizing bacterial symbionts for its nutrition. These are located in a centrally located "trophosome".

Solemya velum, the Atlantic awning clam, is a species of marine bivalve mollusc in the family Solemyidae, the awning clams. This species is found along the eastern coast of North America, from Nova Scotia to Florida and inhabits subtidal sediments with high organic matter (OM) content and low Oxygen, such as salt ponds, salt marshes, and sewage outfalls.

<i>Paracatenula</i> Genus of flatworms

Paracatenula is a genus of millimeter sized free-living marine gutless catenulid flatworms.

<span class="mw-page-title-main">Marine microbial symbiosis</span>

Microbial symbiosis in marine animals was not discovered until 1981. In the time following, symbiotic relationships between marine invertebrates and chemoautotrophic bacteria have been found in a variety of ecosystems, ranging from shallow coastal waters to deep-sea hydrothermal vents. Symbiosis is a way for marine organisms to find creative ways to survive in a very dynamic environment. They are different in relation to how dependent the organisms are on each other or how they are associated. It is also considered a selective force behind evolution in some scientific aspects. The symbiotic relationships of organisms has the ability to change behavior, morphology and metabolic pathways. With increased recognition and research, new terminology also arises, such as holobiont, which the relationship between a host and its symbionts as one grouping. Many scientists will look at the hologenome, which is the combined genetic information of the host and its symbionts. These terms are more commonly used to describe microbial symbionts.

Stilbonematinae is a subfamily of the nematode worm family Desmodoridae that is notable for its symbiosis with sulfur-oxidizing bacteria.

<span class="mw-page-title-main">Hydrothermal vent microbial communities</span> Undersea unicellular organisms

The hydrothermal vent microbial community includes all unicellular organisms that live and reproduce in a chemically distinct area around hydrothermal vents. These include organisms in the microbial mat, free floating cells, or bacteria in an endosymbiotic relationship with animals. Chemolithoautotrophic bacteria derive nutrients and energy from the geological activity at Hydrothermal vents to fix carbon into organic forms. Viruses are also a part of the hydrothermal vent microbial community and their influence on the microbial ecology in these ecosystems is a burgeoning field of research.

<span class="mw-page-title-main">Marine microbiome</span>

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

<span class="mw-page-title-main">Peter Girguis</span> American scientist of microbial symbiosis

Peter R. Girguis is a professor in the department of Organismic and Evolutionary Biology at Harvard University, where he leads a lab that studies animals and microbes that live in extreme environments. He and his lab also develop novel underwater instruments such as underwater mass spectrometers. Girguis was the founder and Chief Technology Officer of Trophos Energy from 2010 to 2012, which focused on commercializing microbial fuel cell technologies. The company was bought by Teledyne Benthos in 2012. Girguis currently serves as a board member of the Ocean Exploration Trust and the Schmidt Marine Technology Partners.

Hydrogen sulfide chemosynthesis is a form of chemosynthesis which uses hydrogen sulfide. It is common in hydrothermal vent microbial communities Due to the lack of light in these environments this is predominant over photosynthesis

<i>Lamellibrachia satsuma</i> Species of tube worms in the family Siboglinidae

Lamellibrachia satsuma is a vestimentiferan tube worm that was discovered near a hydrothermal vent in Kagoshima Bay, Kagoshima at the depth of only 82 m (269 ft) the shallowest depth record for a vestimentiferan. Its symbiotic sulfur oxidizer bacteria have been characterised as ε-Proteobacteria and γ-Proteobacteria. Subspecies have been later found associated with cold seeps at Hatsushima in Sagami Bay and at the Daini Tenryu Knoll in the Nankai Trough with specimens obtained at up to 1,170 m (3,840 ft) depth.

Oligobrachia is a genus in the family Siboglinidae, commonly known as beard worms. These beard worms are typically found at spreading centers, hydrothermal vents, and undersea volcanoes. The siboglinidae are annelids which can be found buried in sediments. Beard worms do not necessarily exist at one specific part of the world's oceans, however, they are spread out all over the ocean floors as long as the surrounding environment is similar; these are known as metapopulations. Most commonly, these organisms are found at the bottom of the ocean floor, whether it be at a depth of roughly 25 meters or hundreds of meters. Oligobrachia can typically be found near hydrothermal vents and methane seeps. An important characteristic of this genus is that it lacks a mouth and gut. Therefore, it relies on symbiotic bacteria to provide the host organism with energy to survive. The majority of oligobrachia that have been observed have been found in the Arctic and other high-latitude areas of the world's oceans.

References

  1. 1 2 3 Bright M, Sorgo A (2003). "Ultrastructural reinvestigation of the trophosome in adults of Riftia pachyptila (Annelida, Siboglinidae)". Invertebrate Biology. 122 (4): 347–368. doi:10.1111/j.1744-7410.2003.tb00099.x.
  2. ↑ Leisch N, Dirks U, Gruber-Vodicka HR, Schmid M, Sterrer W, Ott JA (2011). "Microanatomy of the trophosome region of Paracatenula cf. polyhymnia (Catenulida, Platyhelminthes) and its intracellular symbionts". Zoomorphology. 130 (4): 261–271. doi: 10.1007/s00435-011-0135-y . PMC   3213344 . PMID   22131640.
  3. ↑ "Fig. 1.10 Giant Riftia pachyptila in their habitat and abyssal fauna..." ResearchGate. Retrieved 2020-08-03.
  4. 1 2 3 4 5 6 7 8 9 10 11 12 Eichinger I, Klepal W, Schmid M, Bright M (April 2011). "Organization and microanatomy of the Sclerolinum contortum trophosome (Polychaeta, Siboglinidae)". The Biological Bulletin. 220 (2): 140–53. doi:10.1086/BBLv220n2p140. PMID   21551450. S2CID   22468048.
  5. 1 2 Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (July 1981). "Prokaryotic Cells in the Hydrothermal Vent Tube Worm Riftia pachyptila Jones: Possible Chemoautotrophic Symbionts". Science. 213 (4505): 340–2. Bibcode:1981Sci...213..340C. doi:10.1126/science.213.4505.340. PMID   17819907.
  6. ↑ Claus GW, Roth LE (February 1964). "Fine Structure of the Gram-Negative Bacterium Acetobacter Suboxydans". The Journal of Cell Biology. 20 (2): 217–33. doi:10.1083/jcb.20.2.217. PMC   2106392 . PMID   14126870.
  7. ↑ Dirks U, Gruber-Vodicka HR, Leisch N, Bulgheresi S, Egger B, Ladurner P, Ott JA (2012). "Bacterial Symbiosis Maintenance in the Asexually Reproducing and Regenerating Flatworm Paracatenula galateia". PLOS ONE. 7 (4): e34709. doi: 10.1371/journal.pone.0034709 . PMC   3317999 . PMID   22509347. e34709.
  8. ↑ Rouse GW, Goffredi SK, Vrijenhoek RC (July 2004). "Osedax: bone-eating marine worms with dwarf males". Science. 305 (5684): 668–71. Bibcode:2004Sci...305..668R. doi:10.1126/science.1098650. PMID   15286372. S2CID   34883310.
  9. ↑ Pflugfelder B, Fisher CR, Bright M (2005-04-01). "The color of the trophosome: elemental sulfur distribution in the endosymbionts of Riftia pachyptila (Vestimentifera; Siboglinidae)". Marine Biology. 146 (5): 895–901. doi:10.1007/s00227-004-1500-x. ISSN   0025-3162. S2CID   86203023.
  10. ↑ Wilmot DB, Vetter RD (1990-06-01). "The bacterial symbiont from the hydrothermal vent tubewormRiftia pachyptila is a sulfide specialist". Marine Biology. 106 (2): 273–283. doi:10.1007/BF01314811. ISSN   0025-3162. S2CID   84499903.
  11. ↑ Scott KM, Boller AJ, Dobrinski KP, Le Bris N (2012-02-01). "Response of hydrothermal vent vestimentiferan Riftia pachyptila to differences in habitat chemistry". Marine Biology. 159 (2): 435–442. doi:10.1007/s00227-011-1821-5. ISSN   0025-3162. S2CID   99500443.
  12. 1 2 Klose J, Aistleitner K, Horn M, Krenn L, Dirsch V, Zehl M, Bright M (2016-01-05). Duperron S (ed.). "Trophosome of the Deep-Sea Tubeworm Riftia pachyptila Inhibits Bacterial Growth". PLOS ONE. 11 (1): e0146446. doi: 10.1371/journal.pone.0146446 . PMC   4701499 . PMID   26730960.
  13. ↑ Pflugfelder B, Cary SC, Bright M (July 2009). "Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms". Cell and Tissue Research. 337 (1): 149–65. doi:10.1007/s00441-009-0811-0. PMID   19444472. S2CID   7853776.
  14. ↑ Meylaers K, Clynen E, Daloze D, DeLoof A, Schoofs L (January 2004). "Identification of 1-lysophosphatidylethanolamine (C(16:1)) as an antimicrobial compound in the housefly, Musca domestica". Insect Biochemistry and Molecular Biology. 34 (1): 43–9. doi:10.1016/j.ibmb.2003.09.001. PMID   14723896.
  15. 1 2 Bright M, Keckeis H, Fisher CR (2000-05-19). "An autoradiographic examination of carbon fixation, transfer and utilization in the Riftia pachyptila symbiosis". Marine Biology. 136 (4): 621–632. doi:10.1007/s002270050722. S2CID   84235858.
  16. 1 2 3 Felbeck H, Jarchow J (1998-05-01). "Carbon release from purified chemoautotrophic bacterial symbionts of the hydrothermal vent tubeworm Riftia pachyptila". Physiological Zoology. 71 (3): 294–302. doi:10.1086/515931. PMID   9634176. S2CID   44828316.
  17. ↑ Felbeck H (1983-03-01). "Sulfide oxidation and carbon fixation by the gutless clamSolemya reidi: an animal-bacteria symbiosis". Journal of Comparative Physiology. 152 (1): 3–11. doi:10.1007/BF00689721. ISSN   1432-1351. S2CID   9462221.
  18. ↑ Arndt C, Schiedek D, Felbeck H (1998). "Metabolic responses of the hydrothermal vent tube worm Riftia pachyptila to severe hypoxia". Marine Ecology Progress Series. 174: 151–158. Bibcode:1998MEPS..174..151A. doi: 10.3354/meps174151 . ISSN   0171-8630.
  19. ↑ Sorgo A, Gaill F, Lechaire JP, Arndt C, Bright M (2002). "Glycogen storage in the Riftia pachyptila trophosome: contribution of host and symbionts". Marine Ecology Progress Series. 231: 115–120. Bibcode:2002MEPS..231..115S. doi: 10.3354/meps231115 . ISSN   0171-8630.
  20. 1 2 3 4 5 6 Hinzke T, Kleiner M, Breusing C, Felbeck H, Häsler R, Sievert SM, et al. (December 2019). Ruby D, Distel EG (eds.). "Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis". mBio. 10 (6): e02243–19, /mbio/10/6/mBio.02243–19.atom. doi:10.1128/mBio.02243-19. PMC   6918071 . PMID   31848270.
  21. ↑ Li J, Mahajan A, Tsai MD (December 2006). "Ankyrin repeat: a unique motif mediating protein-protein interactions". Biochemistry. 45 (51): 15168–78. CiteSeerX   10.1.1.502.2771 . doi:10.1021/bi062188q. PMID   17176038.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.