Giant deep-sea tubeworm's meal ticket comes in as a skin infection

Giant tubeworms found near hydrothermal ventsmore than a mile below the ocean surface donot bother to eat: lacking mouth and stomach,they stand rooted to one spot. Fornourishment, they rely completely onsymbiotic bacteria that live within theirbodies to metabolize the sulphurous volcanicsoup in which they both thrive.

But the microscopic larvae of these giantsare born bacteria-free, with a completedigestive system. Juveniles swim, hunt, andeat before permanently settling down andtaking up with their microbial partners. Nowthe idea that the larvae acquire theirsymbionts by eating them has beenoverturned. By collecting the giant worms'tiny spawn from traps laid on the oceanfloor, oceanographers have shown that thesulfur-eating bacteria infect the larvaethrough their skin.

Andrea Nussbaumer and Monika Bright of theUniversity of Vienna, and Charles Fisher,professor of biology at Penn State, reporttheir findings this week in the Britishjournal Nature.

Previous groups had shown that, after a larvaquits swimming and attaches itself to thebottom of the ocean near a volcanic vent, itsmouth disappears and its stomach shrinksaway, even as it grows a specialized organcalled the trophosome that houses thesymbiotic bacteria it collects. "It is anabsolutely obligate symbiosis for the worm,"Fisher explains. "If the larvae do not getthe right symbiont, they die."

The prevailing hypothesis was that theappropriate bacteria were gathered into thestomach during feeding, somehow escapeddigestion, and by remaining in the stomachcaused it to undergo metamorphosis into thetrophosome.

But those conclusions were based on a verysmall set of observations, due to the extremedifficulty of obtaining the tubeworm's larvaland juvenile stages. The only way to collectthese delicate organisms is directly from theocean floor, at 2500 meters depth, in thedeep sea vehicle Alvin. Bright invented"tubeworm artificial settlement cubes," or"baby traps" as the team calls them, tocollect young, just-settled larvae andjuveniles. They left the traps at the bottomnear an active hydrothermal vent and returnedthe next season to collect them, bring themback to land-based laboratories, and analyzethem carefully using molecular techniques andfluorescence- and electron microscopy.

By a painstaking reconstruction of electronmicrographs of thin slices of larvae andjuvenile worms, the team showed that thesymbionts do not enter through the mouth, butthrough the skin, in a process akin toinfection by pathogenic bacteria. Thesebacterial partners then crawl inward, throughvarious larval tissues, not to the stomachbut to an adjacent, "mesodermal" tissue. Upontheir arrival, the bacteria appear to inducethe immature mesodermal tissue todifferentiate and form the trophosome, wherethey proliferate and provide sustenance tothe growing worm indefinitely. In return thebacteria get a safe habitat and a reliablesource of food.

"The symbiont, and only the symbiont, iscapable of invading the skin of the tubewormlarvae. It migrates through several layers oftissue towards the interior of the host, andinto the future trophosome," Brightexplains. "Once the trophosome isestablished, infection ceases, and no furtherinfection appears to be possible at laterstages."

The researchers found that after thetrophosome is established, further infectionappears to be prevented, in part by a wave ofprogrammed cell death in tissues wherestraggling bacteria remain.

"Biologists are realizing that symbiosis isnot an oddity in nature, but rather thenorm," Fisher says. "Most -- if not all --animals and plants exist in symbiosis withsome forms of microbes. We currentlyunderstand the early stages of symbiontacquisition for only a very few of themultitudes of symbioses. Since symbiosis isso widespread, understanding the mechanismsof symbiont acquisition is a first orderquestion for modern biologists."

"In this tubeworm," Bright adds, "thesymbiont acquisition process resembles theinfection processes of pathogenic bacteria.""It may be," Fisher says, "that understandingthe early stages of symbiotic interactionswill help us to understand the early stagesof host-pathogen interactions, andvice-versa."

Source : Penn State