Sea Squids Owe Their Glow to Molecule Previously Linked to Whooping Cough

A molecule that triggers damaging changes in the lungs of children with whooping cough lets a bobtail squid living off the coast of Hawaii acquire the ability to glow, scientists have discovered.

Although the molecule, tracheal cytotoxin (TCT), initially kills certain squid cells, this toxic effect helps the squid build a chamber that will serve as a permanent home for the bacteria inside the squid. The relationship benefits both organisms: the squid give the bacteria a home, and the bacteria allow the squid to glow in a manner that helps them evade predators.

William Goldman, PhD, professor of molecular microbiology at the School of Medicine, originally identified TCT in 1982 in studies of the effects of Bordetella pertussis, the bacteria that causes whooping cough. The molecule is a fragment of peptidoglycan, a component of the bacterial cell wall.

"At the time when we first identified TCT, the concept that a fragment of the cell wall could cause disease pathology was novel and quite controversial," Goldman says. "Now, though, TCT and other molecules like it are widely accepted as triggers of cell damage and immune system responses."

In the years since Goldman identified it, scientists have also linked TCT to damage to the fallopian tubes caused by gonorrhea. But until the discovery of its role in sea squid, published in the November 12, 2004 issue of Science, TCT and other molecules like it had never been linked to beneficial changes.

Goldman, who still studies TCT today, is an author on the study. Other authors include researchers at the University of Hawaii, the University of Iowa, and the University of Georgia. Senior author Margaret McFall-Ngai, PhD, formerly of the University of Hawaii, is now professor of medical microbiology and immunology at the University of Wisconsin at Madison.

In a University of Wisconsin press release, McFall-Ngai cites the finding as evidence of the thin line between beneficial bacteria-host relationships and pathological bacteria-host relationships. According to McFall-Ngai, the finding suggests a need for caution in the use of antibiotic treatments, which kill both harmful and helpful bacteria.

McFall-Ngai and other coauthors who study Euprymna scolopes, a thumb-sized sea squid, approached Goldman about a collaboration because they had found hints that part of peptidoglycan might be playing a role in the squid's interactions with bacteria.

"Like some sea organisms, the bobtail squid houses a luminescent bacterium, Vibrio fischeri, in a specialized structure known as the light organ," Goldman explains. "However, when they're born they have neither a functional light organ nor the glowing bacteria."

After birth, the squid encounter V. fischeri in seawater and work with the bacteria to mature the light organ that will become the bacteria's permanent home. Scientists think the light organ lets the sea squid, which forage by night, wipe out any sea floor shadows that moonlight would otherwise cause them to cast. Lack of a shadow makes the squid less visible to predators.

To confirm the potential link between peptidoglycan and construction of the light organ, McFall-Ngai's lab sent a strain of V. fischeri to Goldman's group. Working together, the groups showed that V. fischeri regularly sheds portions of its cell wall including TCT, and that TCT interacts with lipopolysaccharides, another group of molecules released by the bacteria, to cause the squid tissue changes that mature the light organ.

"The long-term symbiotic relationship that results benefits both the squid and the bacteria," Goldman says. "That's quite a change from what TCT does in the lungs of children."

Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ. Microbial factor-mediated development in a host-bacterial mutualism. Science, November 12, 2004.

Funding from the National Institutes of Health, the W. M. Keck Foundation, and the National Science and Engineering Council of Canada.

Source: Washington University School of Medicine