Life on the edge: A different pathway for infection of Vestimentiferan tubeworms

Vestimentiferan tubeworms live around hydrothermal vents and cold seeps rich in metals. Tubeworms often dominate these ecosystems and are able to colonize rapidly. These animals lack digestive systems and rely on chemoautotrophic bacteria that live endosymbiotically within the worm’s tissues for their nutritional needs. Unlike the adults, Vestimentiferan larvae have a temporary digestive system and initially do not have symbionts. The infection process that the larvae subsequently undergo triggers developmental and physiological changes. Hydrothermal vents are transient and larvae need to be able to travel vast distances to settle on new vents. It is therefore imperative that each new generation of tubeworms becomes infected with symbiotic bacteria.

Previous hypotheses suggested that the symbiotic bacteria entered through the mouth to colonize the dorsal mesentery or midgut. The development of the trophosome from mesodermal tissue would follow, which is an organ containing the symbiotic bacteria in large concentrations. This study by Nussbaumer et al. (2006) suggests that the symbiotic bacteria enter the host through the skin. The bacteria migrate to the dorsal mesentery, where the trophosome forms. The infection process culminates with the digestive system tissue undergoing extensive apoptosis.

The study used devices called tubeworm artificial settlement cubes (TASCs) to aid settlement of larvae and very small juveniles. These cubes were made up of a series of transparent grooved plates that could be taken apart to retrieve the larvae and juveniles. The TASCs were deployed at a hydrothermal vent site within the East Pacific Rise area and retrieved by the submersible Alvin one year later. Three Vestimentiferan species, Riftia pachyptila, Tevnia jerichonana and Oasisia alvinae, had established on the TASCs after one year. These ranged from larvae to juveniles between 200 μm - 2 mm in length. These three species have a very similar symbiotic phylotype. Fluorescent in situ hybridization (FISH) together with electron microscopy were used to confirm that the newly-settled larvae did not have symbionts and had a digestive system upon settlement.

The newly settled larvae appeared to be digesting on the microbes in their guts and it was only when the larvae were 250 μm long, did infection with the symbionts occur. FISH was performed to visualize the infection of the Vestimentiferan trophosome and FISH micrographs showed the symbiotic bacteria entering the larvae through the skin. Depending on the age of the individuals, the bacteria were found in different locations. In larvae and smaller juveniles, rod-shaped bacteria were observed in the dorsal mesentery, the foregut, epidermis, muscles and the cytoplasm but when they were in the trophosome, the bacteria were held within vacuoles. This contrasted with adults and larger juveniles, in which the symbiotic bacteria were found only in the trophosome. No symbionts were detected in the gut lumen, mouth or anus as previous infection hypotheses have suggested.

The authors of this study propose that the infection process begins once the larvae have settled on a substrate and the symbiotic microbes enter the larvae via the skin. They migrate to the dorsal mesentery and there form the trophosome, which expands to fill the digestive cavity. In adult tubeworms, the trophosome occupies the majority of the tube. Newly settled animals released an extracellular mucous which was believed to enable symbionts to colonize the Vestimentiferan larvae.

The authors acknowledge that they did not use live individuals to follow the process of infection and used instead a series of animals of different sizes and developmental stages. Given the environment from which these animals live, I feel it would be difficult to recreate the conditions needed in the lab to observe a live individual from the larval stage to adulthood.  Despite this, I feel that this study has been useful in highlighting that a different developmental pathway for Vestimentiferan symbiont infection is likely and may help answer questions about how the mechanisms for acquisition of microbes in other mutualistic symbioses have evolved.

Reference:

Nussbaumer, A.D., Fisher, C.R. and Bright, M. (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms, Nature, 441, 345-348.

http://www.nature.com/nature/journal/v441/n7091/abs/nature04793.html