Photosynthesis in the Abyss

Rimicaris exoculata is the dominant decapod species found around hydrothermal vents.
Credit: Magnus L. Johnson

Deep-sea hydrothermal vents, with their black smokers, six-foot red tube worms and strange pale crabs and clams have become common features of biology textbooks, mainstream magazines, newspapers and TV nature shows. So has the understanding that these thriving communities depend not on green organisms using the Sun‘s light as a source of energy, but on bacteria and archaea that break down energy-rich chemicals spewing out of the sea floor along with the 350-degree C (662-degree F) vent water.

For more than a decade after the discovery of hydrothermal vent communities in 1977, researchers found no biological evidence of light at vents. But in 1989, Cindy Van Dover, now at The College of William and Mary in Williamsburg, Virginia, began publishing studies of a small eyeless shrimp, Rimicaris exoculata, collected from vent fields in the mid-Atlantic. To their surprise, Van Dover and colleagues found that a patch of tissue on the shrimp’s back contained some of the same pigments found in animal eyes. Calculations showed that the shrimp should be able to detect extremely faint light.

Last year more biological evidence turned up. Robert Jinks and colleagues reported in the November 2002 Nature their studies of a crab with normal eyes as a larva, but nothing more than naked retinas as a vent-dwelling adult. As with the vent shrimp, these crabs cannot see images, but can detect light.

A Crazy Idea

In February 2003, Robert Blankenship, a photosynthesis expert at Arizona State University, added one more organism to the list of vent light users. He reported to the NASA Astrobiology Institute general meeting the results of a search for photosynthetic organisms that he, Van Dover, Jörg Overmann and others carried out during dives to two vent sites in the Pacific.

A magnified image of green sulfur bacteria.
Credit: Lars Juul

"The question that one immediately asks is, ‘Why are you looking for photosynthetic organisms in the deep ocean?’ Because it seems to be sort of a crazy idea. And in fact, it took us quite some time to convince NASA and NSF to support this work," Blankenship says. Even clear ocean water filters out all of the Sun’s light by about 200 meters [650 feet] depth. "But fortunately, the story has a happy ending," Blankenship says.

Using an automated underwater sampling tool, the team sampled water in the plume of a black smoker in a vent field off the coast of Costa Rica nicknamed Nine North (9° north latitude).

Back on the mother ship, Blankenship tested the water with special food, or medium, for a type of bacteria called green sulfur bacteria. "These green sulfur bacteria represent a group of very specialized bacteria," he says. Using a medium for green sulfur bacteria wasn’t a wild guess. Jörg Overmann, at the University of Munich, had previously found green sulfur bacteria deep in the Black Sea.

The Deep, Dark Black Sea

Jörg Overmann has studied green sulfur bacteria growing deep in the cloudy Black Sea since 1988. The first hints that some kind of photosynthetic bacteria grew that deep and dark were traces of the light-capturing chemical bacteriochlorophyll detected by a US-Turkish expedition at about 80 meters [about 260 feet]. From samples of the water brought back by an expedition member, Overmann and colleagues conducted the first analysis of the bacteria..

"At that point, we did not have any molecular data and could not determine the exact composition of the bacterial community," he says. "Photosynthetic activity of the natural samples could not be demonstrated. Also, it remained entirely unclear which light intensities are available in the natural habitat of these green sulfur bacteria."

In December 2001, Overmann had another chance to sample in the Black Sea. "At this occasion, green sulfur bacteria were detected at a depth of 100 m (330 feet), even deeper than before." This time, Overmann was able to grow the bacteria in the lab and learn more about its identity: a member of the green sulfur bacteria usually found in the oxygen-starved waters of estuaries.

In the Black Sea, the Sun remains only the light source for which Overmann sees any evidence. Even with the heavy filtering of the 100 meters (330 feet) of murky water, a tiny amount of visible light remains. In this environment, the bacteria must gather light with great efficiency. A single molecule of bacteriochlorophyll receives a single photon only about once every 8 hours.

Blankenship says of the Black Sea bacteria "These guys are really scrounging for every photon that is there. So in a way it makes sense that that might be the sort of organisms we would find down there at the vents."

Some bacteria are opportunists. They switch between energy sources. If there’s enough light, they carry on photosynthesis to make their own food. If not, they eat whatever food is available in the environment. But for green sulfur bacteria, using light to make food is not an option. They can’t live without light.

Where’s the Light?

Sheri White (above) has measured the light at hydrothermal vents, detecting both infrared light and visible light.
Credit: Monterey Bay Research Institute

Any substance whose temperature is above absolute zero (minus 273 C, minus 460 F]) emits some infrared light, called black body radiation. The hotter the substance, the more black body radiation, and the shorter the wavelength of the light emitted. If the substance is hot enough, the wavelengths get short enough to become red visible light.

You can see the process by switching on an ordinary electric stove. As soon as the element receives power, black body radiation begins to increase, albeit at wavelengths human eyes cannot see. But after a short time, the element begins to glow a dull red, then a brighter red.

Hydrothermal vent water also emits light, mostly in the infrared, and biologists supposed that the vent shrimp detected that light, perhaps to stay near the vent, where they could find food, perhaps to avoid getting too close. The bacteria use near-infrared light, with wavelengths almost into the range of visible red light, to carry on photosynthesis.

Geophysicist Sheri N. White, now at the Monterey Bay Aquarium Research Institute, has measured the light at hydrothermal vents using a specialized camera similar to today’s digital still cameras. These devices use charge coupled devices (CCDs) instead of film to record even a few photons per square centimeter of CCD.

In research done in collaboration with Van Dover and others, White detected the expected infrared radiation. But she also found visible light, albeit dimmer than we can see. The visible light may arise from chemical reactions, the formation and breaking of mineral crystals and from bubble formation.

"So in all vents you see this black body radiation at the long [far red to near infrared] wavelengths. But at some of them you see white light in the visible region," White says. In other vents, particular colors peak. Measurements of visible light from hydrothermal vents put the intensity at about a hundred to a million times dimmer than the light in the Black Sea, depending on which wavelengths are included.

"Now how do these organisms get by on such low light intensities?" Blankenship asks. "They have this wonderful device called a chlorosome." Like a molecular satellite dish, Blankenship says, the chlorosome funnels photons to the molecular machinery that begins the work of storing light energy in the chemical bonds of food molecules.

The chlorosome of vent-dwelling green sulfur bacteria makes them the world champions at garnering photons. (Overmann’s green sulfur bacterium from the Black Sea held the previous record.) It’s unlikely that any other organism that depends on light could get by on fewer photons.

What’s Next?

An estuary, such as this one in Washington, may harbor green sulfur bacteria.
Credit: USGS

Green sulfur bacteria, though common in estuaries, have never been seen before in the open ocean, Blankenship says. Analysis of the new organism’s RNA shows it to be a new species, a close cousin to common estuary green sulfur bacteria, and a close cousin to Overmann’s Black Sea bacteria. Because it’s a clearly a new species, it can’t be a sampling contaminant, Blankenship says. But how long ago the bacteria’s ancestors relocated from higher up in the ocean, settling in a low-oxygen niche near a vent remains an open question.

"There are a lot of unanswered questions," Blankenship says. "One of the things we’re working on right now is to try to look for independent evidence of these organisms using other techniques." Members of the international team are trying to analyze the RNA and DNA in the whole samples they brought back to the lab, a process called environmental PCR, which can detect new organisms even when they can’t be grown in the lab. "So far we haven’t had too much success with that," Blankenship admits, "but we’re just getting going."

"One of the best ways of detecting these things is with their characteristic fluorescence emission." By shining a particular wavelength of light on the bacteria, special instruments can detect the fluorescent glow of their particular photosynthetic pigments. The technical challenge, Blankenship says, is to build an instrument the researchers can put into the water at the hydrothermal vent to measure the fluorescent glow at very close range.

Finally, Blankenship’s group wants to measure how sensitive the new green fluorescent bacteria are to oxygen. All known green sulfur bacteria die in the presence of oxygen. But at vents, the plume of moving water mixes oxygen-containing water with oxygen-free water. A perfectly oxygen-free environment might be hard to find. Perhaps, in addition to adapting to extremely low light, this newly discovered species has also found a way to tolerate small amounts of oxygen.

Related Web Pages

Photosynthesis: Take It of Leave It
Hydrothermal Environments on the Ocean Floor
Life in Extreme Environments