Thursday 17 November 2011

Environmental Uptake of Bacterial Symbionts by Giant Tubeworms

Deep sea hydrothermal vents are dominated by marine invertebrates called tubeworms (Riftia pachyptila). The environments they live in are in complete darkness and very little organic material reaches to these depths. How they manage to maintain their fast growth rate when organic compounds are so scarce was a mystery for many years. After several investigations it was discovered that these animals contain a large internal organ, which was later named the trophosome, instead of a digestive system. The tubeworm uses gills to filter O2, CO2 and H2S from the surrounding water and transports them to the trophosome where Gammaproteobacteria uses them to produce organic molecules for themselves and for their host. The tube worm survival is completely reliant on these chemoautotrophic bacteria but how and where do these bacterial symbionts come from?

A study by Nussbaumer et al (2006) tried to identify how this symbiosis develops. In many obligate symbioses this is achieved via vertical transfer from parent to offspring. However, another unusual discovery was that the larval stage of R. pachyptila did have a digestive system and no trophosome. Transmission electron microscopy and FISH of specimens removed from a hydrothermal vent in the Pacific confirmed there were no symbiotic bacteria present in young larvae. At a certain size of development (250-400μm) the bacteria suddenly appeared. Further evidence suggested that the bacteria entered through the host’s skin rather than through the mouth, almost like an infection. Once inside the bacteria initiated the growth of the trophosome organ and apoptosis of the cells that make up the digestive system.

Harmer et al (2008) tried to further prove the idea that tubeworms acquire their symbiont via environmental uptake rather than vertical transfer. Evidence from other studies have found no evidence of symbiont presence in larvae but whether the bacteria is present in the surrounding environment for up take by tubeworm juveniles was unknown. In this study, samples of seawater and biofilms were collected from the Tica hydrothermal vent in the Pacific Ocean at a depth of ~2,600m. The biofilm samples were collected on bacteria settlement devices that were placed in clusters of R. pachyptila, adjacent to the clusters, 10m and 100m away from the clusters. Sadly, the only water samples taken were 1m away from the clusters. PCR of 16 rRNA and FISH were used to test for the presence of the symbiont. All samples confirmed their presence but with one exception, biofilm samples 100m away from a R. pachyptila which had been collected after only one month. Other samples at this distance that had been left for a year did show symbiont presence. FISH indicated that bacterial abundance was greatest the closer to the clusters, but symbionts were still clearly visible on 100m samples. The authors did comment however, that FISH is only semi-quantitative and so only gave an indication of their numbers.

A number of related papers have been published since these two articles but I picked them because they do high light the very unusual way in which R. pachyptila develops a symbiosis with bacteria from its environment instead of vertical transmission. Without this relationship, the tubeworms would simply not have enough energy to survive.

A Review of:
Harmer, T. Rotjan, R. Nussbaumer, A. Bright, M. Ng, A. DeChaine, E and Cavanaugh, C (2008) Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents. Applied and Environmental Microbiology, 74, 3895-3898.

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

9 comments:

Lee Hutt said...

A very recent investigation by Gardebrecht et al (2011) looked at the metagenomics of sulfur oxidizing bacteria found in R. pachyptila and another tubeworm Tevnia jerichonana. Despite coming from two geochemically different locations, they both share the same species of symbiont and the symbionts are 99.9% homologous regarding key genes. I think this would be a very interesting read but unfortunately I do not think this has been published yet because I cannot get hold of the full article.

Gardebrecht et al (2011) Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. The ISME Journal, ????

Arainna said...

hey, I found this topic really interesting in class when Colin mentioned it, it was nice to read some more about it. I think it's so fascinating/ a little creepy how the bacteria burrow into the host and change the organisms own biochemistry to suit its needs. I know the process results in survival for the host but it makes me think of what was mentioned previously in class about whether the host is being enslaved by its symbiont....in this case I feeling a slight pull towards yes!

valentina sciutteri said...

Hi Lee!I really enjoyed reading this review,this topic is very interesting,i will look for more on web.
The fact that larvae stages have not symbionts is very curious: how is it possible?
To answer this,I think we should look at the physiology of larvae,particularly at their feeding structures;something has to change during their development,as well as in other animals!
The different environmental conditions in which larvae and adults live can also be a critical factor for symbiosis:hydrothermal vents can be very distant among them,and whale carcass have been suggested to be a good site for larval settlement (stepping stone theory) because they share similar conditions.We should investigate microbial communities in both ecocsytems,to know more about this fascinating reality!
Did the authors explain if there were any differences in the community composition among the samples?Is it possible to find a pattern in their distribution?

Lee Hutt said...

Hi guys
Thanks for the comments.
I know what you mean Arainna, its very creepy. It makes you wander if the tubeworms actually have a choose over this colonisation or if it is a kind of infection. The fact that the bacteria can live free in the environment but chooses to switch to a chemolithotrophic symbiosis must mean that its more benifitial for them to do so.

Regarding your question Valentina, sadly the FISH method they used only gives an indication of what species are present but not their distribution. I really hope the article I mentioned above becomes fully avalible soon because it looks into two different species of tubeworms at two very different locations but the symbionts are identical, dispit the long distances between them.

Colin Munn said...

Valentina makes an interesting comment about the 'stepping stone' hypothesis. This has been a bit controversial, I think. There is a recent paper on genetics of Riftia that may be of interst - it's not microbiological, but has some interestign comments on how Riftia colonizes the vent sites.
Here's the URL

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3100261/

Arainna said...

Hey Valentina I've just been reading about whale carcass's being a good site for bacteria along with vents and cold seeps. I don't know if we've read the same paper but I've added the link to this. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0023259

Lee Hutt said...

Hi Arainna
Just checked out that article. Fascinating. I had no idea there was so many of the hydrothermal vents. The map (figure 2) shows really clear patterns, for the cold seeps too. Also interesting how they have tried to divide them into biogeographic provinces. I wander how many more they will find?

valentina sciutteri said...

WOW!Article you suggested are amazing.I think deep sea ecology is fascinating because is so mysterious,like space...I really would like to work on this area in the future...

Joe Murphy said...

Hmm creepy indeed Lee. Very interesting stuff