Euprymna scolopes

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Euprymna scolopes
Euprymna scolopes, South shore of Oahu, Hawaii.tiff
The Hawaiian bobtail squid, Euprymna scolopes, swimming in the water column off the south shore of Oahu
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Mollusca
Class: Cephalopoda
Order: Sepiida
Family: Sepiolidae
Subfamily: Sepiolinae
Genus: Euprymna
Species:
E. scolopes
Binomial name
Euprymna scolopes
Berry, 1913 [2]

Euprymna scolopes, also known as the Hawaiian bobtail squid, is a species of bobtail squid in the family Sepiolidae native to the central Pacific Ocean, where it occurs in shallow coastal waters off the Hawaiian Islands and Midway Island. [3] [4] The type specimen was collected off the Hawaiian Islands and is located at the National Museum of Natural History in Washington, D.C. [5]

Contents

Euprymna scolopes grows to 30 mm (1.2 in) in mantle length. [3] Hatchlings weigh 0.005 g (0.00018 oz) and mature in 80 days. Adults weigh up to 2.67 g (0.094 oz). [6]

In the wild, E. scolopes feeds on species of shrimp, including Halocaridina rubra , Palaemon debilis , and Palaemon pacificus . [7] In the laboratory, E. scolopes has been reared on a varied diet of animals, including mysids ( Anisomysis sp.), brine shrimp ( Artemia salina ), mosquitofish ( Gambusia affinis ), prawns ( Leander debilis ), and octopuses ( Octopus cyanea ). [8]

The Hawaiian monk seal (Monachus schauinslandi) preys on E. scolopes in northwestern Hawaiian waters. [9]

On June 3, 2021, SpaceX CRS-22 launched E. scolopes, along with tardigrades, to the International Space Station. The squid were launched as hatchlings and will be studied to see if they can incorporate their symbiotic bacteria into their light organ while in space. [10]

Symbiosis

Euprymna scolopes lives in a symbiotic relationship with the bioluminescent bacteria Aliivibrio fischeri , which inhabits a special light organ in the squid's mantle. The bacteria are fed a sugar and amino acid solution by the squid and in return hide the squid's silhouette when viewed from below by matching the amount of light hitting the top of the mantle (counter-illumination). [11] E. scolopes serves as a model organism for animal-bacterial symbiosis and its relationship with A. fischeri has been carefully studied. [12] [13] [14] [15] [16] [17] [18] [19]

Acquisition

The bioluminescent bacterium, A. fischeri, is horizontally transmitted throughout the E. scolopes population. Hatchlings lack these necessary bacteria and must carefully select for them in a marine world saturated with other microorganisms. [20]

To effectively capture these cells, E. scolopes secretes mucus in response to peptidoglycan (a major cell wall component of bacteria). [21] The mucus inundates the ciliated fields in the immediate area around the six pores of the light organ and captures a large variety of bacteria. However, by some unknown mechanism, A. fischeri is able to outcompete other bacteria in the mucus. [21]

Adult Euprymna scolopes with scale. Hawaiian Bobtail squid.tiff
Adult Euprymna scolopes with scale.

As A. fischeri cells aggregate in the mucus, they must use their flagella to migrate through the pores and down into the ciliated ducts of the light organ and endure another barrage of host factors meant to ensure only A. fischeri colonization. [21] Besides the relentless host-derived current that forces motility-challenged bacteria out of the pores, a number of reactive oxygen species makes the environment unbearable. [21] Squid halide peroxidase is the main enzyme responsible for crafting this microbiocidal environment, using hydrogen peroxide as a substrate, but A. fischeri has evolved a brilliant counterattack. A. fischeri possesses a periplasmic catalase that captures hydrogen peroxide before it can be used by the squid halide peroxidase, thus inhibiting the enzyme indirectly. [21] Once through these ciliated ducts, A. fischeri cells swim on towards the antechamber, a large epithelial-lined space, and colonize the narrow epithelial crypts. [21]

The bacteria thrive on the host-derived amino acids and sugars in the antechamber and quickly fill the crypt spaces within 10 to 12 hours after hatching. [22]

Ongoing relationship

Every second, a juvenile squid ventilates about 2.6 ml (0.092 imp fl oz; 0.088 US fl oz) of ambient seawater through its mantle cavity. Only a single A. fischeri cell, one/1-millionth of the total volume, is present with each ventilation. [21]

The increased amino acids and sugars feed the metabolically demanding bioluminescence of the A. fischeri, and in 12 hours, the bioluminescence peaks and the juvenile squid is able to counterilluminate less than a day after hatching. [22] Bioluminescence demands a substantial amount of energy from a bacterial cell. It is estimated to demand 20% of a cell's metabolic potential. [22]

Nonluminescent strains of A. fischeri would have a definite competitive advantage over the luminescent wild-type, however nonluminescent mutants are never found in the light organ of the E. scolopes. [22] In fact, experimental procedures have shown that removing the genes responsible for light production in A. fischeri drastically reduces colonization efficiency. [22] Luminescent cells, with functioning luciferase, may have a higher affinity for oxygen than for peroxidases, thereby negating the toxic effects of the peroxidases. [23] For this reason, bioluminescence is thought to have evolved as an ancient oxygen detoxification mechanism in bacteria. [23]

Venting

Despite all the effort that goes into obtaining luminescent A. fischeri, the host squid jettisons most of the cells daily. This process, known as “venting”, is responsible for the disposal of up to 95% of A. fischeri in the light organ every morning at dawn. [24] The bacteria gain no benefit from this behavior and the upside for the squid itself is not clearly understood. One reasonable explanation points to the large energy expenditure in maintaining a colony of bioluminescent bacteria. [25]

During the day when the squid are inactive and hidden, bioluminescence is unnecessary, and expelling the A. fischeri conserves energy. Another, more evolutionarily important reason may be that daily venting ensures selection for A. fischeri that have evolved specificity for a particular host, but can survive outside of the light organ. [26]

Since A. fischeri is transmitted horizontally in E. scolopes, maintaining a stable population of them in the open ocean is essential in supplying future generations of squid with functioning light organs.

Light organ

The light organ has an electrical response when stimulated by light, which suggests the organ functions as a photoreceptor that enables the host squid to respond to A. fischeri's luminescence. [27]

Extraocular vesicles collaborate with the eyes to monitor the down-welling light and light created from counterillumination, so as the squid moves to various depths, it can maintain the proper level of output light. [25] Acting on this information, the squid can then adjust the intensity of the bioluminescence by modifying the ink sac, which functions as a diaphragm around the light organ. [25] Furthermore, the light organ contains a network of unique reflector and lens tissues that help reflect and focus the light ventrally through the mantle. [25]

The light organ of embryonic and juvenile squids has a striking anatomical similarity to an eye and expresses several genes similar to those involved in eye development in mammalian embryos (e.g. eya , dac ) which indicate that squid eyes and squid light organs may be formed using the same developmental "toolkit". [28]

As the down-welling light increases or decreases, the squid is able to adjust luminescence accordingly, even over multiple cycles of light intensity. [25]

See also

Related Research Articles

<span class="mw-page-title-main">Squid</span> Superorder of cephalopod molluscs

A squid is a mollusc with an elongated soft body, large eyes, eight arms, and two tentacles in the superorder Decapodiformes, though many other molluscs within the broader Neocoleoidea are also called squid despite not strictly fitting these criteria. Like all other cephalopods, squid have a distinct head, bilateral symmetry, and a mantle. They are mainly soft-bodied, like octopuses, but have a small internal skeleton in the form of a rod-like gladius or pen, made of chitin.

<span class="mw-page-title-main">Bioluminescence</span> Emission of light by a living organism

Bioluminescence is the production and emission of light by living organisms. It is a form of chemiluminescence. Bioluminescence occurs widely in marine vertebrates and invertebrates, as well as in some fungi, microorganisms including some bioluminescent bacteria, and terrestrial arthropods such as fireflies. In some animals, the light is bacteriogenic, produced by symbiotic bacteria such as those from the genus Vibrio; in others, it is autogenic, produced by the animals themselves.

<span class="mw-page-title-main">Photophore</span> Glandular organ that appears as luminous spots on various marine animals

A photophore is a glandular organ that appears as luminous spots on various marine animals, including fish and cephalopods. The organ can be simple, or as complex as the human eye; equipped with lenses, shutters, color filters and reflectors, however unlike an eye it is optimized to produce light, not absorb it. The bioluminescence can variously be produced from compounds during the digestion of prey, from specialized mitochondrial cells in the organism called photocytes, or, similarly, associated with symbiotic bacteria in the organism that are cultured.

<span class="mw-page-title-main">Bobtail squid</span> Order cephalopod molluscs closely related to cuttlefish

Bobtail squid are a group of cephalopods closely related to cuttlefish. Bobtail squid tend to have a rounder mantle than cuttlefish and have no cuttlebone. They have eight suckered arms and two tentacles and are generally quite small.

<i>Aliivibrio fischeri</i> Species of bacterium

Aliivibrio fischeri is a Gram-negative, rod-shaped bacterium found globally in marine environments. This species has bioluminescent properties, and is found predominantly in symbiosis with various marine animals, such as the Hawaiian bobtail squid. It is heterotrophic, oxidase-positive, and motile by means of a single polar flagella. Free-living A. fischeri cells survive on decaying organic matter. The bacterium is a key research organism for examination of microbial bioluminescence, quorum sensing, and bacterial-animal symbiosis. It is named after Bernhard Fischer, a German microbiologist.

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

Aposymbiosis occurs when symbiotic organisms live apart from one another. Studies have shown that the lifecycles of both the host and the symbiont are affected in some way, usually negative, and that for obligate symbiosis the effects can be drastic. Aposymbiosis is distinct from exsymbiosis, which occurs when organisms are recently separated from a symbiotic association. Because symbionts can be vertically transmitted from parent to offspring or horizontally transmitted from the environment, the presence of an aposymbiotic state suggests that transmission of the symbiont is horizontal. A classical example of a symbiotic relationship with an aposymbiotic state is the Hawaiian bobtail squid Euprymna scolopes and the bioluminescent bacteria Vibrio fischeri. While the nocturnal squid hunts, the bacteria emit light of similar intensity of the moon which camouflages the squid from predators. Juveniles are colonized within hours of hatching and Vibrio must outcompete other bacteria in the seawater through a system of recognition and infection.

Luminescent bacteria emit light as the result of a chemical reaction during which chemical energy is converted to light energy. Luminescent bacteria exist as symbiotic organisms carried within a larger organism, such as many deep sea organisms, including the Lantern Fish, the Angler fish, certain jellyfish, certain clams and the Gulper eel. The light is generated by an enzyme-catalyzed chemoluminescence reaction, wherein the pigment luciferin is oxidised by the enzyme luciferase. The expression of genes related to bioluminescence is controlled by an operon called the lux operon.

<i>Euprymna tasmanica</i> Species of mollusc

Euprymna tasmanica, also known as the southern dumpling squid or southern bobtail squid, is a bobtail squid that lives in the shallow temperate coastal waters of southern Australia's continental shelf. It lives for between 5 and 8 months and the adults can grow up to 6 or 7 cm long with a mantle length of 3 to 4 cm. They are found in seagrass beds or areas with soft silty or muddy bottoms from Brisbane on the east coast to Shark Bay on the west, as well as around Tasmania. Southern dumpling squid are nocturnal and during the day hide in sand or mud covered in a mucus-lined coat of sediment. If disturbed acid glans can quickly remove this coat as an additional decoy to ink squirting.

<i>Sepietta oweniana</i> Species of mollusc

Sepietta oweniana is a common marine mollusc from the order Sepiida, the cuttlefish.

Autoinducers are signaling molecules that are produced in response to changes in cell-population density. As the density of quorum sensing bacterial cells increases so does the concentration of the autoinducer. Detection of signal molecules by bacteria acts as stimulation which leads to altered gene expression once the minimal threshold is reached. Quorum sensing is a phenomenon that allows both Gram-negative and Gram-positive bacteria to sense one another and to regulate a wide variety of physiological activities. Such activities include symbiosis, virulence, motility, antibiotic production, and biofilm formation. Autoinducers come in a number of different forms depending on the species, but the effect that they have is similar in many cases. Autoinducers allow bacteria to communicate both within and between different species. This communication alters gene expression and allows bacteria to mount coordinated responses to their environments, in a manner that is comparable to behavior and signaling in higher organisms. Not surprisingly, it has been suggested that quorum sensing may have been an important evolutionary milestone that ultimately gave rise to multicellular life forms.

Reflectins are a family of intrinsically disordered proteins evolved by a certain number of cephalopods including Euprymna scolopes and Doryteuthis opalescens to produce iridescent camouflage and signaling. The recently identified protein family is enriched in aromatic and sulfur-containing amino acids, and is utilized by certain cephalopods to refract incident light in their environment. The reflectin protein is responsible for dynamic pigmentation and iridescence in organisms. This process is “dynamic” due to its reversible properties, allowing reflectin to change an organism's appearance in response to external factors such as needing to camouflage or send warning signals.

<span class="mw-page-title-main">Cephalopod ink</span> Dark pigment released by cephalopods

Cephalopod ink is a dark-coloured or luminous ink released into water by most species of cephalopod, usually as an escape mechanism. All cephalopods, with the exception of the Nautilidae and the Cirrina, are able to release ink to confuse predators.

<span class="mw-page-title-main">Counter-illumination</span> Active camouflage using light matched to the background

Counter-illumination is a method of active camouflage seen in marine animals such as firefly squid and midshipman fish, and in military prototypes, producing light to match their backgrounds in both brightness and wavelength.

<i>Euprymna berryi</i> Species of mollusc

Euprymna berryi, commonly called hummingbird bobtail squid or Berry's bobtail squid among various other vernacular names, is a species of mollusc cephalopod in the family Sepiolidae.

<span class="mw-page-title-main">Bioluminescent bacteria</span>

Bioluminescent bacteria are light-producing bacteria that are predominantly present in sea water, marine sediments, the surface of decomposing fish and in the gut of marine animals. While not as common, bacterial bioluminescence is also found in terrestrial and freshwater bacteria. These bacteria may be free living or in symbiosis with animals such as the Hawaiian Bobtail squid or terrestrial nematodes. The host organisms provide these bacteria a safe home and sufficient nutrition. In exchange, the hosts use the light produced by the bacteria for camouflage, prey and/or mate attraction. Bioluminescent bacteria have evolved symbiotic relationships with other organisms in which both participants benefit close to equally. Another possible reason bacteria use luminescence reaction is for quorum sensing, an ability to regulate gene expression in response to bacterial cell density.

<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.

<i>Euprymna morsei</i> Species of mollusc

Euprymna morsei, the Mimika bobtail squid, is a species of Indo-Pacific bobtail squid from the family Sepiolidae.

Margaret McFall-Ngai is an American animal physiologist and biochemist best-known for her work related to the symbiotic relationship between Hawaiian bobtail squid, Euprymna scolopes and bioluminescent bacteria, Vibrio fischeri. Her research helped expand the microbiology field, primarily focused on pathogenicity and decomposition at the time, to include positive microbial associations. She currently is a professor at PBRC’s Kewalo Marine Laboratory and director of the Pacific Biosciences Research Program at the University of Hawaiʻi at Mānoa.

Karen Visick is an American microbiologist and expert in bacterial genetics known for her work on the role of bacteria to form biofilm communities during animal colonization. She conducted doctoral research with geneticist Kelly Hughes at the University of Washington, where she identified a key regulatory checkpoint during construction of the bacterial flagellum. She conducted postdoctoral research on development of the Vibrio fischeri-Euprymna scolopes symbiosis with Ned Ruby at University of Southern California and University of Hawaiʻi. The bacteria are bioluminescent and provide light to the host. Visick and Ruby revealed that bacteria that do not produce light exhibit a defect during host colonization.

Ecological evolutionary developmental biology (eco-evo-devo) is a field of biology combining ecology, developmental biology and evolutionary biology to examine their relationship. The concept is closely tied to multiple biological mechanisms. The effects of eco-evo-devo can be a result of developmental plasticity, the result of symbiotic relationships or epigenetically inherited. The overlap between developmental plasticity and symbioses rooted in evolutionary concepts defines ecological evolutionary developmental biology. Host- microorganisms interactions during development characterize symbiotic relationships, whilst the spectrum of phenotypes rooted in canalization with response to environmental cues highlights plasticity. Developmental plasticity that is controlled by environmental temperature may put certain species at risk as a result of climate change.

References

  1. ↑ Barratt, I.; Allcock, L. (2012). "Euprymna scolopes". The IUCN Red List of Threatened Species . 2012: e.T162598A925206. doi: 10.2305/IUCN.UK.2012-1.RLTS.T162598A925206.en . Downloaded on 11 February 2018.
  2. ↑ Julian Finn (2016). "Euprymna scolopes Berry, 1913". World Register of Marine Species. Flanders Marine Institute. Retrieved 11 February 2018.
  3. 1 2 Reid, A. & P. Jereb 2005. Family Sepiolidae. In: P. Jereb & C.F.E. Roper, eds. Cephalopods of the world. An annotated and illustrated catalogue of species known to date. Volume 1. Chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). FAO Species Catalogue for Fishery Purposes. No. 4, Vol. 1. Rome, FAO. pp. 153–203.
  4. ↑ Countries' Exclusive Economic Zones with Euprymna scolopes Archived July 15, 2003, at the Wayback Machine
  5. ↑ "Current Classification of Recent Cephalopoda" (PDF). Archived from the original (PDF) on 2006-01-01. Retrieved 2007-02-16.
  6. ↑ Wood, J.B. & R.K. O'Dor 2000. "Do larger cephalopods live longer? Effects of temperature and phylogeny on interspecific comparisons of age and size at maturity" (PDF). Archived from the original (PDF) on December 14, 2004. (134 KB)Marine Biology136(1): 91.
  7. ↑ Shears, J. 1988. The Use of a Sand-coat in Relation to Feeding and Diel Activity in the Sepiolid Squid Euprymna scolopes. R.T. Hanlon (ed.) Malacologia29(1): 121-133.
  8. ↑ Boletzky, S.v. & R.T. Hanlon. 1983. A Review of the Laboratory Maintenance, Rearing and Culture of Cephalopod Molluscs. Memoirs of the National Museum of Victoria: Proceedings of the Workshop on the Biology and Resource Potential of Cephalopods, Melbourne, Australia, 9–13 March 1981, Roper, Clyde F.E., C.C. Lu and F.G. Hochberg, ed. 44: 147-187.
  9. ↑ Goodman-Lowe, G.D. 1998. "Diet of the Hawaiian monk seal (Monachus schauinslandi) from the northwestern Hawaiian islands during 1991 and 1994" (PDF). Archived from the original (PDF) on May 7, 2005. (294 KB)Marine Biology132: 535-546.
  10. ↑ June 2021, Amy Thompson 01 (June 2021). "SpaceX will launch baby squid and tardigrades to the space station this week". Space.com. Retrieved 2021-06-24.
  11. ↑ Young, R.E. & C.F. Roper 1976. Bioluminescent countershading in midwater animals: evidence from living squid. Science191(4231): 1046–1048. doi : 10.1126/science.1251214
  12. ↑ DeLoney, C.R., T.M. Bartley & K.L. Visick 2002. "Role for phosphoglucomutase in Aliivibrio fischeri-Euprymna scolopes symbiosis" (PDF). Archived from the original (PDF) on March 28, 2004. (221 KB)Journal of Bacteriology184(18): 5121-5129.
  13. ↑ Dunlap, P.V., K. Kitatsukamoto, J.B. Waterbury & S.M. Callahan 1995. "Isolation and characterization of a visibly luminous variant of Aliivibrio fischeri strain ES114 form the sepiolid squid Euprymna scolopes" (PDF). Archived from the original (PDF) on March 28, 2004. (105 KB)Archives of Microbiology164(3): 194-202.
  14. ↑ Foster, J.S., M.A. Apicella & M.J. McFall-Ngai 2000. "Aliivibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes light organ" (PDF). Archived from the original (PDF) on March 28, 2004. (610 KB)Developmental Biology226(2): 242-254.
  15. ↑ Hanlon, R.T., M.F. Claes, S.E. Ashcraft & P.V. Dunlap 1997. "Laboratory culture of the sepiolid squid Euprymna scolopes: A model system for bacteria-animal symbiosis" (PDF). Archived from the original (PDF) on March 28, 2004. (2.38 MB)Biological Bulletin192(3): 364-374.
  16. ↑ Lee, K.-H. & E.G. Ruby 1995. "Symbiotic role of the viable but nonculturable state of Aliivibrio fischeri in Hawaiian coastal seawater" (PDF). Archived from the original (PDF) on March 28, 2004. (249 KB)Applied and Environmental Microbiology61(1): 278-283.
  17. ↑ Lemus, J.D. & M.J. McFall-Ngai 2000. "Alterations in the protoeme of the Euprymna scolopes light organ in response to symbiotic Aliivibrio fischeri" (PDF). Archived from the original (PDF) on March 28, 2004. (2.10 MB)Applied and Environmental Microbiology66: 4091-4097.
  18. ↑ Millikan, D.S. & E.G. Ruby 2003. "FlrA, a s54-Dependent Transcriptional Activator in Aliivibrio fischeri, is required for motility and symbiotic light-organ colonization" (PDF). Archived from the original (PDF) on March 28, 2004. (382 KB)Journal of Bacteriology (American Society for Microbiology) 185(12): 3547-3557.
  19. ↑ Montgomery, M.K. & M. McFall-Ngai 1998. "Late postembryonic development of the symbiotic light organ of Euprymna scolopes (Cephalopoda: Sepiolidae)" (PDF). Archived from the original (PDF) on March 28, 2004. (6.10 MB)Biological Bulletin195: 326-336.
  20. ↑ Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proceedings of the National Academy of Sciences of the United States of America 105(32): 11323-11328. doi : 10.1073/pnas.0802369105
  21. 1 2 3 4 5 6 7 The evolutionary ecology of a sepiolid squid-Aliivibrio association: from cell to environment. Vie et Milieu 58(2): 175-184. ISSN   0240-8759
  22. 1 2 3 4 5 An exclusive contract: Specificity in the Aliivibrio fischeriEuprymna scolopes partnership. Journal of Bacteriology 182(7): 1779-1787. ISSN   0021-9193
  23. 1 2 The evolution of bioluminescent oxygen consumption as an ancient oxygen detoxification mechanism. Journal of Molecular Evolution 52(4): 321-332. ISSN   0022-2844
  24. ↑ Breaking the language barrier: experimental evolution of non-native Aliivibrio fischeri in squid tailors luminescence to the host. Symbiosis51(1): 85-96. doi : 10.1007/s13199-010-0074-2
  25. 1 2 3 4 5 Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca : Cephalopoda). Marine Biology 144(6): 1151-1155. doi : 10.1007/s00227-003-1285-3
  26. ↑ Differentially expressed genes reveal adaptations between free-living and symbiotic niches of Aliivibrio fischeri in a fully established mutualism. Canadian Journal of Microbiology 52(12): 1218-1227. doi : 10.1139/w06-088
  27. ↑ Tong, D., N.S. Rozas, T.H. Oakley, J. Mitchell, N.J. Colley & M.J. McFall-Ngai 2009. Evidence for light perception in a bioluminescent organ. PNAS106(24): 9836–9841. doi : 10.1073/pnas.0904571106
  28. ↑ Peyer, Suzanne M.; Pankey, M. Sabrina; Oakley, Todd H.; McFall-Ngai, Margaret J. (February 2014). "Eye-specification genes in the bacterial light organ of the bobtail squid Euprymna scolopes, and their expression in response to symbiont cues". Mechanisms of Development. 131: 111–126. doi:10.1016/j.mod.2013.09.004. PMC   4000693 . PMID   24157521.

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