Hawaiian Bobtail Squid
Encyclopedia
Euprymna scolopes, also known as the Hawaiian Bobtail Squid, is a species
of bobtail squid
in the family
Sepiolidae
. It is native to the central Pacific Ocean
, where it occurs in shallow coastal waters off the Hawaiian Islands
and Midway Island
. The type specimen was collected off the Hawaiian Islands
and is deposited at the National Museum of Natural History
in Washington, D.C.
.
E. scolopes grows to 30 millimetres (1.2 in) in mantle
length. Hatchlings weigh 0.005 gram (0.00017636981052556 oz) and mature in 80 days. Adults weigh up to 2.67 gram (0.0941814788206489 oz).
In the wild, E. scolopes feeds on species of shrimp
, including Halocaridina rubra, Palaemon debilis, and Palaemon pacificus. 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), prawn
s (Leander debilis), and octopus
es (Octopus cyanea).
The Hawaiian Monk Seal
(Monachus schauinslandi) preys on E. scolopes in northwestern Hawaii
an waters.
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
) . E. scolopes serves as a model organism
for animal-bacterial symbiosis and its relationship with V. fischeri has been carefully studied.
In order to effectively capture these cells, E. scolopes secretes mucus
in response to peptidoglycan
(a major cell wall
component of bacteria
). The mucus inundates the ciliated fields in the immediate area around the 6 pores of the light organ and captures a large variety of bacteria. However, by some unknown mechanism, V. fischeri is able to out-compete other bacteria in the mucus.
As V. fischeri aggregate in the mucus, they must use their flagella to migrate through the pore
s and down into the ciliated ducts of the light organ and endure another barrage of host factors meant to ensure only V. fischeri colonization. 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. Squid halide peroxidase is the main enzyme responsible for crafting this microbiocidal
environment, using hydrogen peroxide
as a substrate, but V. fischeri has evolved a brilliant counterattack. V. fischeri possesses a periplasmic catalase that captures hydrogen peroxide before it can be used by the squid halide peroxidase, thus inhibiting the enzyme indirectly. Once through these ciliated ducts, V. fischeri swim on towards the antechamber, a large epithelial
-lined space, and colonize the narrow epithelial crypts.
The bacteria thrive on the host-derived amino acid
s and sugars in the antechamber
and quickly fill the crypt spaces within 10 to 12 hours after hatching.
through its mantle cavity. Only a single V. fischeri cell, 1 millionth of the total volume, is present with each ventilation.
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 counter-illuminate less than a day after hatching. Bioluminescence demands a substantial amount of energy from a bacterial cell. It’s estimated to demand 20% of a cell’s metabolic potential.
Non-luminescent strains of V. fischeri would have a definite competitive advantage over the luminescent wild-type, however non-luminescent mutants are never found in the light organ of the E. scolopes. In fact, experimental procedures have shown that removing the gene
s responsible for light production in V. fischeri drastically reduces colonization efficiency. It may be that luminescent cells, with functioning luciferase
, have a higher affinity for oxygen
than for peroxidases, thereby negating the toxic effects of the peroxidases. For this reason, bioluminescence is thought to have evolved as an ancient oxygen detoxification mechanism in bacteria.
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.
Since V. fischeri are 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.
Extra-ocular vesicles
collaborate with the eyes to monitor the down-welling light and light created from counter-illumination
, so as the squid moves to various depths it can maintain the proper level of output light. 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
. Furthermore, the light organ contains a network of unique reflector and lens tissues that help reflect and focus the light ventrally through the mantle
.
The light organ of embryo
nic 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 indicates 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.
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
of bobtail squid
Bobtail squid
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...
in the family
Family (biology)
In biological classification, family is* a taxonomic rank. Other well-known ranks are life, domain, kingdom, phylum, class, order, genus, and species, with family fitting between order and genus. As for the other well-known ranks, there is the option of an immediately lower rank, indicated by the...
Sepiolidae
Sepiolidae
Sepiolidae is a family of bobtail squid encompassing 15 genera in three or four subfamilies....
. It is native to the central Pacific Ocean
Pacific Ocean
The Pacific Ocean is the largest of the Earth's oceanic divisions. It extends from the Arctic in the north to the Southern Ocean in the south, bounded by Asia and Australia in the west, and the Americas in the east.At 165.2 million square kilometres in area, this largest division of the World...
, where it occurs in shallow coastal waters off the Hawaiian Islands
Hawaiian Islands
The Hawaiian Islands are an archipelago of eight major islands, several atolls, numerous smaller islets, and undersea seamounts in the North Pacific Ocean, extending some 1,500 miles from the island of Hawaii in the south to northernmost Kure Atoll...
and Midway Island
Midway Atoll
Midway Atoll is a atoll in the North Pacific Ocean, near the northwestern end of the Hawaiian archipelago, about one-third of the way between Honolulu, Hawaii, and Tokyo, Japan. Unique among the Hawaiian islands, Midway observes UTC-11 , eleven hours behind Coordinated Universal Time and one hour...
. The type specimen was collected off the Hawaiian Islands
Hawaiian Islands
The Hawaiian Islands are an archipelago of eight major islands, several atolls, numerous smaller islets, and undersea seamounts in the North Pacific Ocean, extending some 1,500 miles from the island of Hawaii in the south to northernmost Kure Atoll...
and is deposited at the National Museum of Natural History
National Museum of Natural History
The National Museum of Natural History is a natural history museum administered by the Smithsonian Institution, located on the National Mall in Washington, D.C., United States. Admission is free and the museum is open 364 days a year....
in Washington, D.C.
Washington, D.C.
Washington, D.C., formally the District of Columbia and commonly referred to as Washington, "the District", or simply D.C., is the capital of the United States. On July 16, 1790, the United States Congress approved the creation of a permanent national capital as permitted by the U.S. Constitution....
.
E. scolopes grows to 30 millimetres (1.2 in) in mantle
Mantle (mollusc)
The mantle is a significant part of the anatomy of molluscs: it is the dorsal body wall which covers the visceral mass and usually protrudes in the form of flaps well beyond the visceral mass itself.In many, but by no means all, species of molluscs, the epidermis of the mantle secretes...
length. Hatchlings weigh 0.005 gram (0.00017636981052556 oz) and mature in 80 days. Adults weigh up to 2.67 gram (0.0941814788206489 oz).
In the wild, E. scolopes feeds on species of shrimp
Shrimp
Shrimp are swimming, decapod crustaceans classified in the infraorder Caridea, found widely around the world in both fresh and salt water. Adult shrimp are filter feeding benthic animals living close to the bottom. They can live in schools and can swim rapidly backwards. Shrimp are an important...
, including Halocaridina rubra, Palaemon debilis, and Palaemon pacificus. In the laboratory, E. scolopes has been reared on a varied diet of animals, including mysids (Anisomysis sp.), brine shrimp
Brine shrimp
Artemia is a genus of aquatic crustaceans known as brine shrimp. Artemia, the only genus in the family Artemiidae, has changed little externally since the Triassic period...
(Artemia salina
Artemia salina
Artemia salina is a species of brine shrimp – aquatic crustaceans that are more closely related to Triops and cladocerans than to true shrimp. It is a very old species that does not appear to have changed in .-Description:...
), mosquitofish
Mosquitofish
The mosquitofish is a species of freshwater fish, also commonly, if ambiguously, known by its generic name, gambusia. It is sometimes called the western mosquitofish, to distinguish it from the eastern mosquitofish . It is a member of the family Poeciliidae of order Cyprinodontiformes...
(Gambusia affinis), prawn
Prawn
Prawns are decapod crustaceans of the sub-order Dendrobranchiata. There are 540 extant species, in seven families, and a fossil record extending back to the Devonian...
s (Leander debilis), and octopus
Octopus
The octopus is a cephalopod mollusc of the order Octopoda. Octopuses have two eyes and four pairs of arms, and like other cephalopods they are bilaterally symmetric. An octopus has a hard beak, with its mouth at the center point of the arms...
es (Octopus cyanea).
The Hawaiian Monk Seal
Hawaiian Monk Seal
The Hawaiian monk seal, Monachus schauinslandi, is an endangered species of earless seal in the Phocidae family that is endemic to the Hawaiian Islands....
(Monachus schauinslandi) preys on E. scolopes in northwestern Hawaii
Hawaii
Hawaii is the newest of the 50 U.S. states , and is the only U.S. state made up entirely of islands. It is the northernmost island group in Polynesia, occupying most of an archipelago in the central Pacific Ocean, southwest of the continental United States, southeast of Japan, and northeast of...
an waters.
Symbiosis
E. scolopes lives in a symbioticSymbiosis
Symbiosis is close and often long-term interaction between different biological species. In 1877 Bennett used the word symbiosis to describe the mutualistic relationship in lichens...
relationship with the bioluminescent bacteria
Bacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
Vibrio fischeri
Vibrio fischeri
Vibrio fischeri is a gram-negative rod-shaped bacterium found globally in marine environments. V. fischeri has bioluminescent properties, and is found predominantly in symbiosis with various marine animals, such as the bobtail squid. It is heterotrophic and moves by means of flagella. Free living...
, which inhabits a special light organ in the squid's mantle. The bacteria are fed a sugar
Sugar
Sugar is a class of edible crystalline carbohydrates, mainly sucrose, lactose, and fructose, characterized by a sweet flavor.Sucrose in its refined form primarily comes from sugar cane and sugar beet...
and amino acid
Amino acid
Amino acids are molecules containing an amine group, a carboxylic acid group and a side-chain that varies between different amino acids. The key elements of an amino acid are carbon, hydrogen, oxygen, and nitrogen...
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
Counter-illumination
Counterillumination is a method of camouflage in which bioluminescent light from within an organismon the ventral surface is matched to the light radiating from the environment. The bioluminescent is used to obscure the organism's silhouette produced by the down-welling light. Some midwater...
) . E. scolopes serves as a model organism
Model organism
A model organism is a non-human species that is extensively studied to understand particular biological phenomena, with the expectation that discoveries made in the organism model will provide insight into the workings of other organisms. Model organisms are in vivo models and are widely used to...
for animal-bacterial symbiosis and its relationship with V. fischeri has been carefully studied.
Acquisition
The bioluminescent bacterium, V. 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.In order to effectively capture these cells, E. scolopes secretes mucus
Mucus
In vertebrates, mucus is a slippery secretion produced by, and covering, mucous membranes. Mucous fluid is typically produced from mucous cells found in mucous glands. Mucous cells secrete products that are rich in glycoproteins and water. Mucous fluid may also originate from mixed glands, which...
in response to peptidoglycan
Peptidoglycan
Peptidoglycan, also known as murein, is a polymer consisting of sugars and amino acids that forms a mesh-like layer outside the plasma membrane of bacteria , forming the cell wall. The sugar component consists of alternating residues of β- linked N-acetylglucosamine and N-acetylmuramic acid...
(a major cell wall
Cell wall
The cell wall is the tough, usually flexible but sometimes fairly rigid layer that surrounds some types of cells. It is located outside the cell membrane and provides these cells with structural support and protection, and also acts as a filtering mechanism. A major function of the cell wall is to...
component of bacteria
Bacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
). The mucus inundates the ciliated fields in the immediate area around the 6 pores of the light organ and captures a large variety of bacteria. However, by some unknown mechanism, V. fischeri is able to out-compete other bacteria in the mucus.
As V. fischeri aggregate in the mucus, they must use their flagella to migrate through the pore
Pore
- Animal biology and microbiology :* Sweat pore, an anatomical structure of the skin of humans used for secretion of sweat* Canal pore, an anatomical structure that is part of the lateral line sense system of some aquatic organisms...
s and down into the ciliated ducts of the light organ and endure another barrage of host factors meant to ensure only V. fischeri colonization. Besides the relentless host-derived current that forces motility
Motility
Motility is a biological term which refers to the ability to move spontaneously and actively, consuming energy in the process. Most animals are motile but the term applies to single-celled and simple multicellular organisms, as well as to some mechanisms of fluid flow in multicellular organs, in...
-challenged bacteria out of the pores, a number of reactive oxygen species makes the environment unbearable. Squid halide peroxidase is the main enzyme responsible for crafting this microbiocidal
Microbicide
Microbicides for sexually transmitted diseases, are pharmacologic agents and chemical substances that are capable of killing or destroying certain microorganisms that commonly cause human infection, for example the human immunodeficiency virus....
environment, using hydrogen peroxide
Hydrogen peroxide
Hydrogen peroxide is the simplest peroxide and an oxidizer. Hydrogen peroxide is a clear liquid, slightly more viscous than water. In dilute solution, it appears colorless. With its oxidizing properties, hydrogen peroxide is often used as a bleach or cleaning agent...
as a substrate, but V. fischeri has evolved a brilliant counterattack. V. fischeri possesses a periplasmic catalase that captures hydrogen peroxide before it can be used by the squid halide peroxidase, thus inhibiting the enzyme indirectly. Once through these ciliated ducts, V. fischeri swim on towards the antechamber, a large epithelial
Epithelium
Epithelium is one of the four basic types of animal tissue, along with connective tissue, muscle tissue and nervous tissue. Epithelial tissues line the cavities and surfaces of structures throughout the body, and also form many glands. Functions of epithelial cells include secretion, selective...
-lined space, and colonize the narrow epithelial crypts.
The bacteria thrive on the host-derived amino acid
Amino acid
Amino acids are molecules containing an amine group, a carboxylic acid group and a side-chain that varies between different amino acids. The key elements of an amino acid are carbon, hydrogen, oxygen, and nitrogen...
s and sugars in the antechamber
Antechamber
An antechamber is a smaller room or vestibule serving as an entryway into a larger one. The word is formed of the Latin ante camera, meaning "room before"....
and quickly fill the crypt spaces within 10 to 12 hours after hatching.
Ongoing relationship
Every second a juvenile squid ventilates about 2.6 millilitre (2.340023400234E-10 imp fl oz) of ambient seawaterSeawater
Seawater is water from a sea or ocean. On average, seawater in the world's oceans has a salinity of about 3.5% . This means that every kilogram of seawater has approximately of dissolved salts . The average density of seawater at the ocean surface is 1.025 g/ml...
through its mantle cavity. Only a single V. fischeri cell, 1 millionth of the total volume, is present with each ventilation.
The increased amino acids and sugars feed the metabolically
Metabolism
Metabolism is the set of chemical reactions that happen in the cells of living organisms to sustain life. These processes allow organisms to grow and reproduce, maintain their structures, and respond to their environments. Metabolism is usually divided into two categories...
demanding bioluminescence
Bioluminescence
Bioluminescence is the production and emission of light by a living organism. Its name is a hybrid word, originating from the Greek bios for "living" and the Latin lumen "light". Bioluminescence is a naturally occurring form of chemiluminescence where energy is released by a chemical reaction in...
of the V. fischeri and in 12 hours the bioluminescence peaks and the juvenile squid is able to counter-illuminate less than a day after hatching. Bioluminescence demands a substantial amount of energy from a bacterial cell. It’s estimated to demand 20% of a cell’s metabolic potential.
Non-luminescent strains of V. fischeri would have a definite competitive advantage over the luminescent wild-type, however non-luminescent mutants are never found in the light organ of the E. scolopes. In fact, experimental procedures have shown that removing the gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
s responsible for light production in V. fischeri drastically reduces colonization efficiency. It may be that luminescent cells, with functioning luciferase
Luciferase
Luciferase is a generic term for the class of oxidative enzymes used in bioluminescence and is distinct from a photoprotein. One famous example is the firefly luciferase from the firefly Photinus pyralis. "Firefly luciferase" as a laboratory reagent usually refers to P...
, have a higher affinity for oxygen
Oxygen
Oxygen is the element with atomic number 8 and represented by the symbol O. Its name derives from the Greek roots ὀξύς and -γενής , because at the time of naming, it was mistakenly thought that all acids required oxygen in their composition...
than for peroxidases, thereby negating the toxic effects of the peroxidases. For this reason, bioluminescence is thought to have evolved as an ancient oxygen detoxification mechanism in bacteria.
Venting
Despite all the effort that goes forth into obtaining luminescent V. fischeri, the host squid jettison 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. 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.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.
Since V. fischeri are 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 that the organ functions as a photoreceptor that enables the host squid to respond to V. fischeris luminescence.Extra-ocular vesicles
Vesicle (biology)
A vesicle is a bubble of liquid within another liquid, a supramolecular assembly made up of many different molecules. More technically, a vesicle is a small membrane-enclosed sack that can store or transport substances. Vesicles can form naturally because of the properties of lipid membranes , or...
collaborate with the eyes to monitor the down-welling light and light created from counter-illumination
Counter-illumination
Counterillumination is a method of camouflage in which bioluminescent light from within an organismon the ventral surface is matched to the light radiating from the environment. The bioluminescent is used to obscure the organism's silhouette produced by the down-welling light. Some midwater...
, so as the squid moves to various depths it can maintain the proper level of output light. Acting on this information, the squid can then adjust the intensity of the bioluminescence
Bioluminescence
Bioluminescence is the production and emission of light by a living organism. Its name is a hybrid word, originating from the Greek bios for "living" and the Latin lumen "light". Bioluminescence is a naturally occurring form of chemiluminescence where energy is released by a chemical reaction in...
by modifying the ink sac
Ink sac
With the exception of nocturnal and very deep water cephalopods, all coeloids which dwell in light conditions have an ink sac, which can be used to expel a cloud of dark ink to confuse predators. This sac is a muscular bag which originated as an extension of the hind gut...
, which functions as a diaphragm around the light organ
Light organ
A light organ is an electronic device which automatically converts an audio signal such as music into rhythmic light effects. In the 1970s, light organs were a popular lighting effect used in discotheques and dance parties...
. Furthermore, the light organ contains a network of unique reflector and lens tissues that help reflect and focus the light ventrally through the mantle
Mantle (mollusc)
The mantle is a significant part of the anatomy of molluscs: it is the dorsal body wall which covers the visceral mass and usually protrudes in the form of flaps well beyond the visceral mass itself.In many, but by no means all, species of molluscs, the epidermis of the mantle secretes...
.
The light organ of embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...
nic and juvenile squids has a striking anatomical similarity to an eye and expresses
Gene expression
Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product. These products are often proteins, but in non-protein coding genes such as ribosomal RNA , transfer RNA or small nuclear RNA genes, the product is a functional RNA...
several genes similar to those involved in eye development in mammalian embryos (e.g. eya
EYA1
Eyes absent homolog 1 is a protein that in humans is encoded by the EYA1 gene.-Further reading:...
, dac
DACH1
Dachshund homolog 1 , also known as DACH1, is a protein which in humans is encoded by the DACH1 gene.- Function :This gene is similar to the D. melanogaster dachshund gene, which encodes a nuclear factor essential for determining cell fates in the eye, leg, and nervous system of the fly...
) which indicates that squid eyes and squid light organs may be formed using the same developmental
Developmental biology
Developmental biology is the study of the process by which organisms grow and develop. Modern developmental biology studies the genetic control of cell growth, differentiation and "morphogenesis", which is the process that gives rise to tissues, organs and anatomy.- Related fields of study...
"toolkit".
As the down-welling light increases or decreases, the squid is able to adjust luminescence accordingly, even over multiple cycles of light intensity.
Further reading
- Callaerts, P., P.N. Lee, B. Hartmann, C. Farfan, D.W.Y. Choy, K. Ikeo, K.F. Fischbach, W.J. Gehring & G. de Couet 2002. PNAS 99(4): 2088-2093.