Euprymna scolopes

Euprymna scolopes
The Hawaiian bobtail squid, Euprymna scolopes, swimming in the water column off the south shore of Oahu
Scientific classification
Kingdom: Animalia
Phylum: Mollusca
Class: Cephalopoda
Order: Sepiolida
Family: Sepiolidae
Subfamily: Sepiolinae
Genus: Euprymna
Species: E. scolopes
Binomial name
Euprymna scolopes
Berry, 1913

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.[1][2] The type specimen was collected off the Hawaiian Islands and is deposited at the National Museum of Natural History in Washington, D.C..[3]

Euprymna scolopes grows to 30 mm (1.2 in) in mantle length.[1] Hatchlings weigh 0.005 g (0.00018 oz) and mature in 80 days. Adults weigh up to 2.67 g (0.094 oz).[4]

In the wild, E. scolopes feeds on species of shrimp, including Halocaridina rubra, Palaemon debilis, and Palaemon pacificus.[5] 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).[6]

The Hawaiian monk seal (Monachus schauinslandi) preys on E. scolopes in northwestern Hawaiian waters.[7]

Symbiosis

Euprymna scolopes lives in a symbiotic relationship with the bioluminescent bacteria Vibrio 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).[8] E. scolopes serves as a model organism for animal-bacterial symbiosis and its relationship with V. fischeri has been carefully studied.[9][10][11][12][13][14][15][16]

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.[17]

To effectively capture these cells, E. scolopes secretes mucus in response to peptidoglycan (a major cell wall component of bacteria).[18] 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.[18]

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.[18] 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.[18] 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.[18] Once through these ciliated ducts, A. fischeri cells swim on towards the antechamber, a large epithelial-lined space, and colonize the narrow epithelial crypts.[18]

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.[19]

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 V. fischeri cell, one/1-millionth of the total volume, is present with each ventilation.[18]

The increased amino acids and sugars feed the metabolically demanding bioluminescence of the V. fischeri, and in 12 hours, the bioluminescence peaks and the juvenile squid is able to counterilluminate less than a day after hatching.[19] Bioluminescence demands a substantial amount of energy from a bacterial cell. It is estimated to demand 20% of a cell’s metabolic potential.[19]

Nonluminescent strains of V. 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.[19] In fact, experimental procedures have shown that removing the genes responsible for light production in V. fischeri drastically reduces colonization efficiency.[19] Luminescent cells, with functioning luciferase, may have a higher affinity for oxygen than for peroxidases, thereby negating the toxic effects of the peroxidases.[20] For this reason, bioluminescence is thought to have evolved as an ancient oxygen detoxification mechanism in bacteria.[20]

Venting

Despite all the effort that goes into obtaining luminescent V. 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 V. fischeri in the light organ every morning at dawn.[21] 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.[22]

During the day when the squid are inactive and hidden, bioluminescence is unnecessary, and expelling the V. fischeri conserves energy. Another, more evolutionarily important, reason may be that daily venting ensures selection for V. fischeri that have evolved specificity for a particular host, but can survive outside of the light organ.[23]

Since V. 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 V. fischeri's luminescence.[24]

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.[22] 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.[22] Furthermore, the light organ contains a network of unique reflector and lens tissues that help reflect and focus the light ventrally through the mantle.[22]

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".

As the down-welling light increases or decreases, the squid is able to adjust luminescence accordingly, even over multiple cycles of light intensity.[22]

See also

References

  1. 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.
  2. ↑ Countries' Exclusive Economic Zones with Euprymna scolopes Archived July 15, 2003, at the Wayback Machine.
  3. ↑ Current Classification of Recent Cephalopoda
  4. ↑ 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). (134 KB) Marine Biology 136(1): 91. Archived December 14, 2004, at the Wayback Machine.
  5. ↑ 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.) Malacologia 29(1): 121-133.
  6. ↑ 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.
  7. ↑ Goodman-Lowe, G.D. 1998. "Diet of the Hawaiian monk seal (Monachus schauinslandi) from the northwestern Hawaiian islands during 1991 and 1994." (PDF). (294 KB) Marine Biology 132: 535-546. Archived May 7, 2005, at the Wayback Machine.
  8. ↑ Young, R.E. & C.F. Roper 1976. Bioluminescent countershading in midwater animals: evidence from living squid. Science 191(4231): 1046–1048. doi:10.1126/science.1251214
  9. ↑ DeLoney, C.R., T.M. Bartley & K.L. Visick 2002. "Role for phosphoglucomutase in Aliivibrio fischeri-Euprymna scolopes symbiosis." (PDF). (221 KB) Journal of Bacteriology 184(18): 5121-5129. Archived March 28, 2004, at the Wayback Machine.
  10. ↑ 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). (105 KB) Archives of Microbiology 164(3): 194-202. Archived March 28, 2004, at the Wayback Machine.
  11. ↑ 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). (610 KB) Developmental Biology 226(2): 242-254. Archived March 28, 2004, at the Wayback Machine.
  12. ↑ 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). (2.38 MB) Biological Bulletin 192(3): 364-374. Archived March 28, 2004, at the Wayback Machine.
  13. ↑ Lee, K.-H. & E.G. Ruby 1995. "Symbiotic role of the viable but nonculturable state of Aliivibrio fischeri in Hawaiian coastal seawater." (PDF). (249 KB) Applied and Environmental Microbiology 61(1): 278-283. Archived March 28, 2004, at the Wayback Machine.
  14. ↑ 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). (2.10 MB) Applied and Environmental Microbiology 66: 4091-4097. Archived March 28, 2004, at the Wayback Machine.
  15. ↑ 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). (382 KB) Journal of Bacteriology (American Society for Microbiology) 185(12): 3547-3557. Archived March 28, 2004, at the Wayback Machine.
  16. ↑ Montgomery, M.K. & M. McFall-Ngai 1998. "Late postembryonic development of the symbiotic light organ of Euprymna scolopes (Cephalopoda: Sepiolidae)." (PDF). (6.10 MB) Biological Bulletin 195: 326-336. Archived March 28, 2004, at the Wayback Machine.
  17. ↑ 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
  18. 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
  19. 1 2 3 4 5 An exclusive contract: Specificity in the Aliivibrio fischeri Euprymna scolopes partnership. Journal of Bacteriology 182(7): 1779-1787. ISSN 0021-9193
  20. 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
  21. ↑ Breaking the language barrier: experimental evolution of non-native Aliivibrio fischeri in squid tailors luminescence to the host. Symbiosis 51(1): 85-96. doi:10.1007/s13199-010-0074-2
  22. 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
  23. ↑ 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
  24. ↑ 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. PNAS 106(24): 9836–9841. doi:10.1073/pnas.0904571106

Further reading

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