Features: May 2001

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A Hawaiian bobtail squid owes its luminescence to Vibrio fischeri bacteria housed in an internal light organ. The bacteria secrete a chemical that, when it has accumulated in sufficient concentration, stimulates them to glow.

Bacteria have adapted to a huge range of environments on earth, surviving and multiplying in and on plants and animals, in rock layers deep beneath the surface, in searing desert soils, under polar ice, and under extremely high temperatures and pressures in thermal vents on the ocean floor. During the past decade, we have begun to realize that the success of these tiny, single-celled organisms may depend in large part on their ability to converse with one another using chemical signals. Cell-to-cell communication allows bacteria to coordinate their activity and thus enjoy benefits otherwise reserved for multicellular organisms.

By means of a process called quorum sensing, bacteria are able to detect when they are assembled in large numbers as opposed to when they are essentially alone. They may then adjust their behavior accordingly. Bacteria alert one another to their presence by releasing chemical molecules known as autoinducers. When a chemical of this type becomes sufficiently concentrated in the environment (for example, in an organ such as the lungs or intestinal tract), bacteria that are sensitive to it respond by turning on genes that regulate the production of certain proteins. The newly manufactured proteins, in turn, affect the behavior of the bacteria, which take advantage of one another's presence in their efforts to survive and proliferate.

Until recently, the exchange of chemical signals was assumed to be a trait characteristic of "higher" multicellular organisms. Researchers knew of only a few cases of bacterial cell-to-cell communication and considered them the exception rather than the rule. But now scientists are realizing that this capacity is not only common but critical for bacterial survival and interaction in natural habitats.

The phenomenon of quorum sensing was first discovered in two species of bioluminescent marine bacteria, Vibrio fischeri and V. harveyi. Both of these glow-in-the-dark organisms produce light only when their quorum-sensing ability notifies them that they have reached a high cell density. They then manufacture luciferase, an enzyme concoction that facilitates a light-producing biochemical reaction. Although the two species are quite closely related, they inhabit very different niches in the ocean. V. fischeri lives in symbiotic association with a number of marine animals, producing light that host animals use for such purposes as luring prey, scaring off predators, and attracting mates. In return, V. fischeri gets to reside in the hosts' specialized light organs, where it is provided with amino acids and other nutrients. V. harveyi, by contrast, is a free-living organism, and no one has yet figured out what advantage it derives from emitting light.

One of V. fischeri's most fascinating associations is with certain bobtail squids of the genus Euprymna, the best studied being the Hawaiian bobtail squid. Living in knee-deep coastal waters, this small creature buries itself in the sand during the day and comes out to hunt after dark. Its lifestyle makes the squid especially vulnerable to predation on clear, bright nights, when light shining on the animal from the moon and stars could cause it to cast a shadow and tip off predators patrolling beneath it. But through an alliance with V. fischeri, the squid has evolved a light organ that serves as a camouflaging mechanism. The amount of light emitted from this organ, located on the underside of the creature's body, is controlled by an iris-like structure. The squid senses the intensity of light from the sky and regulates its light organ accordingly, so that the animal, seen from below, more or less matches the background.

The squid's light is produced by the symbiotic bacteria inhabiting the light organ. After a baby squid hatches, V. fischeri bacteria in the seawater swim through ducts leading into the immature light organ, where the hospitable conditions enable them to multiply. There the bacteria live suspended in fluid and, as part of their normal behavior, secrete an autoinducer (the chemical that signals their presence) into it. The bacteria interpret a threshold concentration of this chemical as their cue to switch on the production of light. In effect, V. fischeri bacteria alert one another that they are inside a suitable host. When dispersed in the ocean water, however, the bacteria and their autoinducer chemicals never reach critical concentrations. Then again, the bacteria probably do not gain anything by emitting light outside the squid.

A remarkable part of this exquisite symbiosis is the way the squid keeps the bacterial culture fresh within its light organ. At sunrise, when the squid prepares to bury itself in the sand for a day of sleep, so many bacterial cells are living in its light organ that the animal cannot supply them all with adequate nutrients. The squid circumvents this problem by pumping out about 95 percent of the V. fischeri. This also reduces the level of autoinducer in the light organ below the critical threshold and causes the bacteria remaining within to stop producing light. The pumping is tuned to the squid's circadian rhythm and is activated only at sunrise. As the day goes by, the bacteria begin to divide, their numbers increase, and more autoinducer accumulates. By nightfall, the light organ is "on" again, ready to do its job.