Science: Bacterial 'Harpoon' Triggers Tubeworm Metamorphosis

A novel form of interaction between bacteria and tubeworms prompts the worms to switch from free-swimming larvae to sedentary juveniles, researchers report.
Bacteria are the key to turning free-swimming tubeworm larvae into sedentary juveniles, which collect on ship hulls and ocean drilling rigs. | Science/AAAS

Before some bottom-dwelling marine organisms like the Hydroides elegans tubeworm can make their messy homes on the hulls of ships, they have to interact with bacteria to make the switch from a free-swimming larval state to a stationary juvenile. But, until now, researchers have gone without glimpsing the details of these enigmatic dances between the two organisms.

A new study shows that when it comes to this particular tubeworm and the Pseudoalteromonas luteoviolacea bacterium, the bacterium brandishes a unique array of tail-like structures that may inject the cues for metamorphosis directly into the tubeworm larvae.

This exchange, a unique form of interaction between animals and bacteria, could help researchers understand how marine bacterial biofilms are able to trigger the development of certain sea creatures.

Nicholas Shikuma from the California Institute of Technology along with colleagues from Howard Hughes Medical Institute and the University of Hawaii, report this discovery in the 10 January issue of Science.

"Knowledge of this bacterium-tubeworm system, which was pioneered by [co-author] Michael Hadfield's team in Hawaii, may lead to a better understanding of - and possibly inhibition of - biofouling, or the accumulation of organisms on man-made structures," said Shikuma. "The biofouling of ships' hulls increases drag in the water and ups the ships' fuel consumption."

Cal Tech and Howard Hughes researchers Martin Pilhofer and Gregor Weiss used a technique known as electron cryotomography, which allows for high-resolution, three-dimensional images of biological samples that are frozen in lifelike states, to reveal how P. luteoviolacea turns on the tubeworm's metamorphosis. They were surprised to discover that the bacteria harbored this array of phage tail-like structures, linked together by tail fibers and a unique hexagonal net.

It's this complicated and previously unrecognized feature that prompts the tubeworm to develop past its larval stage, they say. But the researchers don't know exactly what the structure does to the tubeworm to trigger its metamorphosis.

Based on their similarity to other bacterial toxin secretion systems, "these structures may have originally evolved as weapons," suggested Grant Jensen, a co-author of the Science paper. "They're organized in a 'loaded' but tightly compacted state within the cell and then expand like an umbrella or a flower, opening up into a large mine field of spear guns, ready to fire."

Dianne Newman, another co-author of the Science paper, was a bit more cautious when discussing the team's findings. "[The weapons angle] is a very reasonable hypothesis," she said. "But the evolutionary history of this class of structures is an interesting open question."

Regardless of their origin, the researchers have dubbed the harpoon-like structures metamorphosis-associated contractile structures, or MACs. "But my favorite way to refer to them around the lab is to call them 'Big Macs,'" joked Newman.

"There are likely entirely novel classes of these contractile tail-like assemblies for bacteria," according to Pilhofer. "And it's possible that reengineered synthetic versions could have improved characteristics regarding their use as drug delivery vehicles or anti-bacterial agents."

For now, their exact functions remain unknown. But it's clear that the tubeworm's larvae cannot develop without some help from these bacterial Big MACs.