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imageWhat I want to do today is talk with you about a number of animals, from three different habitats that live in the presence of a toxic gas, hydrogen sulfide. Hydrogen sulfide is a naturally occurring compound. It smells like rotten eggs. If you walk out on the mud flats, you'll smell it. It occurs in many different environments. The interesting thing about hydrogen sulfide, biologically, is that it is a highly toxic molecule. It is toxic on the same level as cyanide. It is toxic because it binds to iron. There are two important iron atoms in biological systems. One is at the center of the hemoglobin molecule. So, typically in the presence of hydrogen sulfide oxygen transport by hemoglobin is blocked and can no longer go on. The second and more ubiquitous problem with hydrogen sulfide is that it binds to the iron at the center of cytochrome molecules, Cytochromes, of course, are the basis of aerobic respiration. So any animal that is aerobically poised in their metabolism in the presence of sulfide, barring special adaptations, will be unable to utilize molecular oxygen as the basis for their metabolism.

Hydrogen Sulfide Detoxification

imageThere are a number of animals that are tolerant of sulfide and can live in sulfide rich environments. Several strategies that could be employed for the tolerance of sulfide include:

  1. The exclusion of sulfide from the body surface, which typically is not seen in nature because sulfide is a very small molecule. It easily diffuses across membranes, particularly respiratory surfaces which are the site of toxicity.

  2. It is theoretically possible that animals could evolve sulfide insensitive cytochrome, some molecular variation of cytochrome which is insensitive. This has not been shown to date.

  3. Animals can also employ anaerobic metabolism. Now this is a very real possibility because many animals, marine invertebrates are anaerobic in their metabolism, at least part of the time, that is they can continue to respire, metabolize and be active in the absence of oxygen. If an animal is able to get by without oxygen, molecular oxygen as an energy source, then it doesn't matter if sulfide is around because their poisoning of aerobic metabolism isn't of concern.

  4. video button sound button  The fourth theoretical strategy for tolerating sulfide and one which I have spent most of my career investigating is sulfide detoxification, by either binding it and removing it from harms way, or chemically converting it to another compound that is no longer a toxic molecule.

And what I want to show you today is a number of animals living in different habitats that have evolved rather elaborate mechanisms for the detoxification of sulfide, and therefore are able to exploit and flourish in what we would consider inhospitable environments.

imageThree environments I want to visit with you: First of all, the hydrothermal vent environment at the bottom of the ocean. This is a very remote habitat. It is 2.5 Km in depth at the bottom of the ocean. Hydrogen sulfide levels there are quite high greater than l millimolar in concentration. I should mention that sulfide is toxic at the nanomolar level, so millimolar concentrations are quite high. The second site, that I want to visit with you is the cold seep environment. This is a more shallow environment, 600 meters to 800 meters in depth. It's characterized by lower levels of hydrogen sulfide, but they can get quite high, so somewhere between zero and one millimolar. We visit this site with the use of the bubble submarine, the Johnson Sea Link, shown here in diagrammatic form. Thirdly, we will go to the sea level environment, our own backyard and we will look at mud flat animals. In general, basically at the surface of the earth, there are a number of environments that are rich in sulfide. The marine mud flat is one. There are many marshes that have elevated levels of hydrogen sulfide and also sewer outfalls, pump mill effluents - there are a number of industrial environments that are very enriched in sulfide as well that are occupied by large colonies of animals.

Two of the environments that I want to take you to are shown on this map. Along the Galapagos rift and at 21deg; north are hydrothermal vent sites along the east Pacific rise. The second environment I mentioned, the seep environment, is in the Gulf of Mexico. This is the site I just returned from a couple of weeks ago.

Hydrothermal Vents

video button sound button  Let's start at the hydrothermal vent environment. First of all, we are at the very bottom of the ocean at 2.5 kilometers in depth. The hydrothermal vents were discovered in 1977. They were discovered by a group of geologists that were exploring the phenomenon of plate shifting at the earth's crust, at the earth's surface. What happens here is that due to plate shifting, there are fissures that open up in the earth's surface. The ambient bottom water is sucked down into the cracks and goes down toward the center of the earth and comes in contact with the hot molten magma at the center of the earth, is superheated and then is forcibly discharged back into the environment through the ocean floor.

There are two general types of hydrothermal vents. One is the diffuse venting environment where water percolates out at a slightly lower rate. Temperature of this water is 10-20°C. Typical bottom temperature of the ocean is about 2°C. So this water is elevated in temperature. In the so called black smoker environment of the hydrothermal vents, water issuing forth from the chimney is as high as 350°C. So this is a very dynamic, very temperature elevated environment. The other important aspect of the venting activity of this percolating flow of fluid into this environment is that as the water moves from the core out into the sea floor, it becomes laden with inorganic chemicals. Hydrogen sulfide in particular, as you know is my emphasis, is taken up by the water at depth so that water discharging into the environment is enriched in hydrogen sulfide.

Regardless of the hydrogen sulfide enriched environment, elevated temperatures, and the dynamic volcanic activity, there are animals that cluster around these sites. It was really a remarkable discovery for scientists just 20 years ago and at the time was really quite startling because most of the deep sea is quite a barren environment and is characterized by soft sediment. There is not a lot of substrate for animals to build their habitats on. So here, all of a sudden, scientists came across an environment where there was hard substrate pillow lava, rock basically for animals to adhere to. There are elevated temperatures and a great deal of biological life. So the idealized vent environment includes pillow lava here in the foreground, sort of a rocky substrate and clams that are wedged into the fissures between the pillow lava. As you get in closer to the vent proper, there are tubeworms, there are white smoker chimneys and black smoker chimnies with the hot water percolating out and a lot of free ranging animals roaming in and out of the vent environment, Brachyuran crabs, Galatheid crabs, several species of fish and a host of other animals.

image video button sound button Here is an actual shot from depth of the pillow lava showing the vesicomyid clam. This is a fairly large clam, Calyptogena magnifica. They get to be about 8-10 inches in length. A very large animal, they wedge their feet down into the cracks of the rock, and this is their microhabitat within the vent environment.


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