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imageOK, I want to turn to Riftia in some detail. I've spent a good deal of my career looking at the physiology of this animal and asking questions about how it manages to live in this sulfide enriched environment, both how it deals with sulfide toxicity and also how it deals with the metabolic usage of the hydrogen sulfide gas by its internal symbiotic bacteria. imageTo give you a little bit of an idea of what this animal is all about, looking at the morphology, again there is the respiratory plume which is the portion that sticks out of the end of the chitinous tube which is not shown in this diagram. There is a collar-like vestamentum organ which positions the animal within the tube, and then there is a large trunk region of the animal, in fact it's a little bit shortened in this particular diagram, and that trunk is filled with only basically two things. There is huge organ called the trophosome. This organ is believed to be the vestigial gut and is composed, literally, of masses of bacteria all enclosed in membrane. So it is a large, dense organ that fills almost the entire trunk, the entire coelom of the animal and it basically just billions of bacteria all grouped together. They have taken over....it is as if your entire body were taken over by a bunch of bacteria...which isn't a good thing to think about probably, but for this animal it works. In addition to the trophosomes there is come coelomic fluid that bathes it, just free fluid in this compartment. It's rich in hemoglobin, the respiratory pigment hemoglobin, and also I should mention that the animal has an elaborate circulatory system similar to ours. And, this circulatory system is a closed circulatory system. It is powered by a heart like structure in the vestimentum region. It pumps blood from the respiratory plume to the region of the bacteria where there are elaborate capillary beds...a very sophisticated blood circulatory system. The red color in the blood is due to hemoglobin and that gives the characteristic red color of the plumes. That's why the plumes are red, because of the very high concentration of hemoglobin that is present in their circulatory system.

imageI have done a great deal of work on the respiratory hemoglobin over the years. One of my focuses is the biochemistry and the function of respiratory pigments in terms of transport of metabolites and metabolic gases.

In the case of Riftia, the key respiratory gases, the key metabolic gases involved are, of course, oxygen, hydrogen sulfide and carbon dioxide. Those are the principle building blocks for the metabolism of the symbiotic bacteria. What we were able to show is that the respiratory pigment present in the plume of the animal is capable of binding oxygen and hydrogen sulfide simultaneously with a very high affinity and keeping it in a tightly bound state transforming it to the center region of the animal where it is off loaded to the bacteria which utilizes it for metabolism.

There are two important considerations about this finding. One is that hydrogen sulfide is necessary for the metabolism of the bacteria so in order to get it from the surrounding water to the site of the metabolism of the bacteria, the idea of a transport molecule is very functional and has worked quite well for this animal. More important in terms of the detoxification of sulfide, these animals are utilizing sulfide for their metabolism, but they also have tissues that are highly sensitive to sulfide, just like our tissues are, so the detoxification aspect of this binding of sulfide is that if hydrogen sulfide is present in the atmosphere, in this case the water, it is bound very rapidly and very tightly to the respiratory hemoglobin, and therefore is kept out of harms way from the rest of the tissues. So it is basically sopped up and kept from interacting with other tissues....body wall tissues, or other aerobically poised tissues.

Riftia and other hydrothermal vent organisms are aerobic organisms. That is, they utilize oxygen as the basis of their metabolism. They are not relying on anaerobic metabolism in order to survive the sulfide.So this is a beautiful adaptation in the sense that it functions for gas transport, and for metabolism, and it also functions for detoxification or tolerance of what would be a very inhospitable environment for most animals.

imageThis is the basic diagram of what is going on in the animal. To reiterate, the chemosynthetic pathway in Riftia involves the uptake of hydrogen sulfide and oxygen and carbon dioxide binding to the respiratory hemoglobin in the plume and transport to the bacteria which are housed in the trophosome organ in the trunk of the animal. Then, what is happening in this bacteria is that hydrogen sulfide is oxidized, in the presence of oxygen, and that energy released from the oxidation pathway is used to run the Calvin-Benson cycle. And that Calvin-Benson cycle functions to fix inorganic carbon dioxide into organic molecules that are then translocated, leaked out to the animal tissue. And, obviously this happens in great order and with many, many, many bacteria. Such that it can fuel and provide nutrients for very large, robust, active animals in this particular environment.

imageAnother issue that I am very interested in is what kinds of microhabitats animals seek out and how they manage to exploit them. This is a kind of a perfect scenario here, in that the worms anchor themselves in the rocks where the hydrothermal vent fluid is issuing out into the sea floor, so at the base of their tube hydrothermal fluid is entering into the environment. It's enriched in hydrogen sulfide and CO2, but is devoid of oxygen. Temperatures are fairly elevated right here, but there is a gradient across the animal which is of interest physiologically, as well. Temperature is a big player in metabolism. And the plumes, the respiratory surface, is extended up into the ambient bottom water which is 2°C in temperature and is devoid of hydrogen sulfide and enriched in oxygen. So it's essential for these animals to seek out the interface between the hydrothermal fluids and the ambient bottom water. So they seek that interface and they're restricted to an area where there is a combination of both of these characteristics. Then these metabolites are taken up by the plume and transported to the interior region of the animal for metabolism.

imageWithout going into great detail, I also want to mention that the hydrothermal vent clam, the large clam that we looked at employs a similar strategy....similar, but different. That's what you'll find, that generally all these animals have interesting stories, that have some similarities, but everybody has a new little spin on it. So these guys basically position themselves, as I mentioned, in cracks in the pillow lava. They wedge their muscular foot down into the region where the hydrothermal plume is percolating out. It's enriched in hydrogen sulfide and elevated in temperature. They point their siphon end up into the ambient bottom water and they take in oxygen and carbon dioxide through the siphon. So they are taking up hydrogen sulfide across the foot and carbon dioxide and oxygen into the siphon region. They also, interestingly, are enriched in hemoglobin. These clams have a high concentration of hemoglobin in their blood which isn't unique although you don't open a common clam and find it with a lot of hemoglobin in it, but there are many surface dwelling clams that do have hemoglobin. But, there is a high concentration of it and it is very actively involved in oxygen binding and also sulfide binding for transport of important metabolic gases to internal symbiants in the gill region.

imageOK, leaving the hydrothermal vent environment, then, and traveling to the seep environment...again the seep environment is a more shallow environment---600 to 800 meters is typically the range of depths that we see. To remind you, the seep environment that I have been involved with the exploration of, is in the Gulf of Mexico which is naturally enriched environment. There is a lot of hydrocarbon and petroleum, that has been trapped in the sediments over geological time. There are also seep environments present in the Monterey Bay and various other places. They are beginning to be discovered elsewhere as well.

Cold Seeps

The cold seep environment as opposed to the hydrothermal environment is a soft sediment environment. There is no volcanic activity going on here. It is quite a different kind of geological environment. The soft sediment has some of the same compounds present and present some of the same physiological challenges to animals because there are high concentrations of hydrogen sulfide present here. There is methane percolating out from the surface of the earth, and also there are pools of brine that occur in this environment. It is quite an interesting environment.

imageWe visit this environment with the use of the submersible the Johnson Sea Link. imageThe Johnson Sea Link is a wonderful submarine. It's run out of Harbor Branch Oceanographic Institution in Fort Pierce, Florida. It's different from Alvin. It has its pluses and minuses. The biggest plus to Johnson Sea Link is that it is a Plexiglas sphere. So rather than sitting in this cramped titanium sphere where you have a tiny little porthole to look out, this whole structure is basically a giant sphere. You sit very comfortably, well you are a little cramped, but at least you sit, on a chair, and basically you have sort of the whole environment out in front of you. So, it is a much more comfortable and a much more useful tool in order to be able to see the range of environments and the magnitude of the environment. The problem with the Johnson Sea Link and submarines of this type is that they are depth limited because of the Plexiglas nature versus the titanium sphere. But for our purposes in the Gulf where it is 600 to 800 meters this is a very functional submarine. We do two dives a day. Basically it takes about four hours per dive and so it quite a comfortable way to work. Again you see here the biobox where we collect our animals. This is a vacuum collector so they can turn on a vacuum and basically suck animals out from the bottom. Cameras, videocameras housed on the submarine and a whole slew of the equipment and technology. Quite fascinating.

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