Twinkiling Bobtail Squids

In the marine environment, symbiosis is a very common association between two or more organisms. Since this vast habitat can sometimes be quite inhospitable, organisms adapt to living in a positive relationship between each other. In fact, one of the most known, and probably most studied, examples is surely the symbiotic relationship between a polyp and zooxanthellae (a microalgae that lives within the polyp’s tissue).

However, there are many more of these interesting associations out there, one of which is the symbiosis between the Hawaiian bobtail squid (Euprymna scolopes) and a γ-proteobacterium Vibrio fischeri. The bobtail squid lives within the coastal shallow waters of Hawaii Islands. It is a nocturnal predator and thanks to the symbiosis with the bioluminescent Vibrio fischeri uses counterillumination as a tactic of predation. Vibrio fischeri, on the other hand, is not a free-living bacterial species, so finding a host is an essential quest.

The bobtail squid juveniles do not contain any bacteria in their luminescent organs. Growing up, however, they acquire the bacteria through ventilation. Approximately each second, there is one Vibrio fischeri cell that enters into the squid’s cloak cavity and continues its path through the pores (there are six in total)  found on the surface of the luminescent organ.

Credit: Mattias Ormestad

In order to establish the symbiosis, there must be some ground mechanisms for the capture of Vibrio fischeri. 1) Laterally to the luminescent organ, the appendages must have a ciliated epithelium. 2) After the squid is born, the capture is first permissive and becomes restrictive, followed by a specific crypt’s colonization. 3) Above the luminescent organ’s pores, a mucus is produced in response to the components of the bacterial cell wall. 4) The bacterium has to move and apply a chemotactic response.

After a few hours from the meeting, Vibrio fischeri enters through the pores, passes through the luminescent organ’s ducts to finally colonize the crypts. Only then, the luminescent organ matures and becomes functional. Mucus is not produced anymore, the ciliate epithelium retracts and goes into a process of cell death called apoptosis, the ducts become thinner, there is a density increase of the microvilli of the epithelial cells within the crypts, and finally, mucus is produced within.

The squids’ luminescent organ maturates thanks to the perception of the bacterial cell wall components, such as peptidoglycan and lipopolysaccharide. The colonization is also possible thanks to the capacity of the bacterium to surpass physical and chemical barriers and, most importantly, the immune system of the host. It is suspected that this could be the reason why a different bacterial species is not able to colonize the bobtail squid.

There are some ways through which Euprymna scolopes combats the colonization by Vibrio fischeri. In the ducts, it moves the epithelial cilia outwords and produces toxic concentrations of nitric oxide (NO). V. fischeri, however, moves fast, produces chemotactic stimuli and possesses systems that inactivate NO. In the crypts, Euprymna scolopes defends itself by hemocytes with phagocytic activity and production of a peroxidase. Again, V. fischeri scores 2-2 by establishing a specific interaction with ligand – microvilli receptor and production of catalysis.

V. fischeri multiplies within 10-12 hours and is able to fill the cryptic spaces, where it becomes highly abundant (1011 cells/mL), producing bioluminescence. One day after the birth of E. scolopes, juveniles are already able to emit light. The bacterial cells that cannot produce bioluminescence due to mutations of the gene lux are immediately eliminated. The fast growing Euprymna scolopes suggests that Vibrio fischeri is able to obtain nutrients.

Each day, 90-95%  of the bacteria is expelled from the luminescent organ, whereas the remaining 5-10% repopulates the crypts within a day. It is important that the symbionts are expelled because in doing so, the Hawaiian bobtail squid controls the number of bacteria, keeps a young population of Vibrio fischeri in a constant exponential growth state, does not waste energy throughout the day and, finally, offers a bacterial inoculum for its juveniles.

Such a profound and specific symbiotic association suggests a coevolutionary trajectory of these two organisms. It is only one example of such symbiosis, imagine knowing more of them!

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