Symbiont shifts in deep-sea mussels

Bathymodiolus, a genus of deep-sea mussels found in hydrothermal vents and cold seeps worldwide, are colonised by chemosynthetic bacteria, obtained from the surrounding environment at an early life stage. As these symbionts oxidise sulphur and methane, it is thought they provide the mussels with additional nutrients. However the exact process through which colonisation occurs is unknown and was the aspect this study aimed to investigate.

Samples of B. azoricus and B. puteoserpentis (juveniles measuring between 4-21mm) were collected from two hydrothermal vents in the Mid-Atlantic Ridge located 3000km apart. Semi-thick sections of the whole juvenile were analysed using FISH to determine the distribution and specificity of symbionts colonising these two species of mussels. Three probes were used: a symbiont specific probe; a general eubacterial probe and a negative probe.

The symbiont specific probe revealed sulphur and methane oxidising symbionts in the gills of all samples. The smallest of the mussels also demonstrated these in the epithelial cells of the retractor muscle, mantle and foot. Overall, the gills showed the densest colonisation of symbionts. There was overlap between the symbiont specific probe and eubacterial probe in all samples, suggesting that these specific symbionts are the only colonising bacteria on the juvenile mussels. Furthermore, they found that the larger juveniles had symbionts only on their gills. To determine whether this was also true for adult Bathymodiolus they carried out further analysis on the mantle tissue attached to the gills of adult B. azoricus (measuring 55-100mm), and found symbionts only on the gills.

This was the first study that used FISH to prove that symbionts colonise a range of epithelial tissues of mussels at an early life stage, providing further evidence to support previous research that also stated this. They believe this to be an unusual occurrence since most other studies have demonstrated symbiosis to be limited to a specific tissue even at an early life stage. Since the gills develop after the foot and mantle, it is believed the reason for such widespread colonisation is due to the provision of additional nutrients for the mussel. Nonetheless, Bathymodiolus are filter feeders, so could use this alone to obtain a sufficient amount of nutrients, suggesting the symbionts colonising the foot and mantel may actually be irrelevant.  

They found the shift of the symbionts became restricted to the gill bacteriocytes when the mussels were at the developmental stage between 8.4-9mm. Since the foot and mantle epithelia are not directly next to the hemolymph lacuna, like the bacteriocytes of the gills, the symbionts are not able to supply a sufficient amount of nutrients in relation to the costs of maintaining them. This therefore provides a suitable explanation to the benefits of the symbionts being retained only in the gills. Furthermore, the large surface area and cilial ventilation of the gills means they can supply oxygen and reduced compounds required by the symbionts. Despite this, juveniles measuring less than 9mm have a thin layer of non-gill epithelia, which is sufficient in providing the requirements of the symbionts, and it was unclear of the difference that would make this insufficient in adult mussels. The paper then reveals that the early stage Bathymodiolus may simply be yet to have developed an immune system capable of preventing indiscriminate infection by the symbionts. Therefore, further study is required to understand the role of the immune system and the benefits the symbionts supply to the host in order to determine the exact process of colonisation and how this is maintained. 

http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej20135a.html

Shift from widespread symbiont infection of host tissues to specific colonisation of gills in juvenile deep-sea mussels 

Cecilila Wentrup, Annelie Wendeberg, Julie Y Huang, Christian Borowski and Nicole Dubilier