Life without Light: Discoveries from the Abyss
by Robin Meadows
The depths of the sea were once believed to be nearly as devoid of life as the moon. A mile and a half below the ocean's surface, the ambient water was thought to be always cold because no sunlight can penetrate so deep. Those creatures hauled up from these dark reaches were considered scarce and believed to subsist largely on organic material drifting down from above.
At least that is what many scientists thought until 1977, when two geologists descended 8,200 feet into the ocean near the Galapagos Islands. The geologists were looking for a deep sea hot spring or hydrothermal vent, which they had predicted to exist along rifts, areas where the sea floor is spreading apart and where volcanic activity and superheated water were likely to occur. Lava wells up through the rifts, forming new crust and heating the water that percolates down through cracks in the crust. Hydrothermal vents then spew this hot water back into the sea [see Smoking in the Dark].
As expected, they found the first vent, an area about 100 meters across where 60F water "streamed out of every orifice and crack in the sea floor," says Massachusetts Institute of Technology geologist John Edmond. But they also made a completely unexpected discovery: The vent was jammed with animals.
"Here we came upon a fabulous scene," says Edmond. "Reefs of mussels and fields of giant clams...along with crabs, anemones, and large pink fish." Both the 10-inch clams and the blind crabs scuttling about were porcelain white, in stark contrast to the otherwise barren black basalt of the newly formed ocean floor surrounding the vent. The other-worldliness of the scene was heightened by the fact that the most common animal was the giant tubeworm, a six-foot invertebrate that extends feathery, bright red plumes from the top of its chitinous white tube.
Biologists were astonished. "I got a call...from the chief scientist...who said he had discovered big clams and tubeworms, and I simply didn't believe it. He was a geologist after all," said Woods Hole Oceanographic Institution biologist Holger Jannasch to Time magazine.
The serendipitous discovery of vent life raised many puzzling questions, perhaps the most perplexing of which was, what were these animals living on? Most living things get their energy from sunlight. Plants photosynthesize and so depend directly on the sun for their energy, and animals eat plants or plant-eating animals and so depend indirectly on the sun for their energy. But what was the source of energy here in the deep, dark depths of the sea? Figuring out what the giant tubeworms (Riftia pachptila) lived on was especially mystifying because they had no mouths, guts, or anuses!
This last question was answered in 1980, when then-Harvard graduate student Colleen Cavanaugh had a wild idea that turned out to be right. Answering the question of the vent life's energy source actually turned out to be relatively straightforward. The water spurting from hydrothermal vents is full of hydrogen sulfide and other energy-rich compounds. Before the discovery of the Galapagos vent, it was well known that terrestrial sulfur springs are home to bacteria that get their energy by oxidizing the sulfide in the water. These bacteria thus get their energy by chemosynthesis rather than photosynthesis.
Likewise, hydrothermal vents are teeming with sulfide-oxidizing bacteria. The bacteria grow in thick, white-to-yellow-to-pink mats that cover all the hard surfaces around the vents from rocks to clam shells to tubeworm tubes. As abundant as the bacteria are above the vents, however, scientists believe that even more grow in pores below the rocky surface. "Occasionally blooms of...bacteria become so dense they create a whiteout, a patchy bacterial blizzard," says biologist Cindy Lee Van Dover of Duke University.
Many of the animals living at vents eat these sulfide-oxidizing bacteria--the first case of animals that depend on chemosynthesis rather than photosynthesis for their ultimate source of energy. "One of the most significant events in the earth and life sciences in this century was the realization that hydrothermal activity can support life in the absence of sunlight," says Van Dover.
But what of the mouthless, gutless giant tubeworms? They obviously weren't eating bacteria. The prevailing hypothesis was that they were absorbing tiny particles of food through their skin. This method of "eating" had originally been proposed for their cousins, hair-sized tubeworms that also lack mouths and guts. First found in 1900, these tubeworms are so small that they could theoretically absorb all the food they need across their skin. The giant tubeworms, however, are so big that they would not be able to get enough nutrients using this method because their surface area relative to their body size is smaller.
This mystery began to unravel when Harvard's Cavanaugh had a flash of insight at a graduate seminar on the giant tubeworms. She was watching Meredith Jones, then curator of worms at the Smithsonian Institution, give a slice-by-slice tour of a giant tubeworm that had been cut like a salami. When Jones reached a slice of the trophosome, an organ of then-unknown function that dominated the inside of the tubeworm--extending along 75 percent of its length--he mentioned that he had seen sulfur crystals in this organ.
"At this point, I jumped up and said, 'It's perfectly clear that tubeworms have symbiotic sulfide-oxidizing bacteria,'" recalls Cavanaugh, explaining that elemental sulfur is the most common intermediate of sulfide-oxidizing bacteria. "[Jones] essentially said, 'Sit down, kid, we think the trophosome is a detoxifying organ.'" The detoxification hypothesis had been proposed because the levels of sulfide and other minerals in vent waters are so high that they would be fatal to most animals.
When asked if other biologists initially thought she was nuts, Cavanaugh, who is now on the faculty at Harvard, laughs and responds with a resounding, "yes!" But the idea made perfect sense to her. Cavanaugh was familiar with sulfide-oxidizing bacteria because before starting graduate school, she had spent two years studying the ecology of a sulfide-rich salt marsh near the Marine Biological Laboratory in Woods Hole, on the coast of Cape Cod.
Her conviction that the giant tubeworms had symbiotic bacteria was so strong that she persisted and got a sample of giant tubeworm tissue from Jones. With the help of other biologists, Cavanaugh stunned the scientific community by showing that tubeworms did indeed harbor bacteria inside their trophosome cells. In fact, bacteria comprise the bulk of trophosome tissue. Other researchers showed that the trophosome contained enzymes characteristic of sulfide-oxidizing bacteria that are not found in animal cells.
Symbiosis is a partnership that can result in two (or more) species essentially functioning as a "new organism" that can thrive in an environment where neither species would flourish alone. In this case, the tubeworm gets a source of food in the nutrient-poor depths of the ocean, although it is not yet clear whether the tubeworms live on bacterial excretions or dead bacterial cells. And the bacteria get a guaranteed supply of sulfide: A tubeworm collects the compound with its red plumes and delivers it to the bacteria via sulfide-binding proteins in its blood.
While this was the first known case of an animal with chemosynthetic bacteria living in its cells, the concept was not as far-fetched as it might sound. Scientists had known for years that many corals and sea urchins have photosynthetic algae living within their cells. And studies also indicate that mitochondria, the energy-producing parts of all plant and animal cells, evolved from free-living bacteria [see Aliens in Our Cells].
While going from two separate organisms to a single symbiotic organism seems like a big jump, this transition undoubtedly took place by degrees. First, free-living bacteria probably started living on the tubeworms' skin. Next, the bacteria probably began living under the skin and finally within tubeworm cells. In support of this theory, Cavanaugh cites living examples of these intermediate steps: nematodes that have bacteria living on them, and oligochaetes (segmented worms) that have sulfide-oxidizing bacteria living under their cuticles.
Ironically, although these symbioses were first found at a deep sea hydrothermal vent, biologists have since found that they exist widely in far more accessible environments. As it happened, Cavanaugh found the next animal with symbiotic bacteria in its cells near Woods Hole, where biologists have been studying marine creatures since the 1800s.
"I'd been thinking about sulfur and bacteria a lot, and I thought 'why not chemosynthetic symbiosis wherever there's sulfur?'" says Cavanaugh. After finishing her tubeworm work, she turned her attention to a clam, Solemya velum, that lives in sulfide-rich eelgrass beds. Clams in the genus Solemya had long been a mystery because their guts are either extremely small or non-existent, and their feeding appendages are too short to reach outside the shell. While Solemya velum does have a small gut, Cavanaugh found that this clam could not possibly eat enough to sustain itself.
In light of her discovery of what tubeworms live on, she was not at all surprised to find that Solemya velum had symbiotic bacteria within the cells of its gills. Subsequent research showed that the 10-inch white clams from the Galapagos vent and most other vent molluscs also have symbiotic bacteria in their gills, which are unusually thick and fleshy.
Today biologists believe that such symbioses exist in more than 100 species of marine invertebrates, including the tiny tubeworms originally thought to subsist on food absorbed through their skin. All these animals live in sulfide-containing environments from mudflats to sewage outfalls to petroleum-laced sediments.
While most of the known chemosynthetic symbionts depend on sulfide for their energy, many other energy-rich compounds could support symbioses between aquatic animals and bacteria. These compounds include methane, manganese, and ammonia. Recently Cavanaugh and other researchers have determined that several marine invertebrates have symbiotic bacteria that get their energy from methane, which is found in many environments from hydrothermal vents to cold-seeps, cold springs in the Gulf of Mexico and the North Sea.
These species include two mussels from the Gulf of Mexico, a hair-sized tubeworm found off the coast of Denmark, and a mussel from a vent along the Mid-Atlantic Ridge. This vent mussel is particularly intriguing because it may also have sulfide-oxidizing bacteria, which would allow the mollusc to take advantage of whichever energy source was more abundant at a given time. "It's unprecedented to maintain a stable symbiosis with two kinds of bacteria," notes Cavanaugh.
The discovery of the hydrothermal vents and the wondrous creatures they sustain shows that despite millennia of study, the world around us still holds surprises. The depths of the sea remain largely unexplored--99 percent of the sea floor has yet to be mapped--and there's bound to be plenty more hot stuff down there.
Robin Meadows is a contributing editor to ZooGoer.
(ZooGoer 25(3) 1996. Copyright 1996 Robin Meadows. All rights reserved.)
