The Light at the Bottom of the Sea

Two miles below the surface of the sea, a mysterious glow emerges from cracks in the Earth. In that glow, the first steps to photosynthesis may have taken place, 3.8 billion years ago.

By Zimmer|Friday, November 01, 1996
Once it seemed that the ocean floor was a desert of darkness. As everyone knew, sunlight was what made life possible by fueling photosynthesis, and sunlight can penetrate only the first few hundred yards of the ocean’s great depths. Lower, a few creatures might still eke out a living by scrounging the organic detritus that drifts down from the surface of the sea. But thousands of feet down, in the utter blackness at the ocean’s bottom, there could be practically nothing.

Then, in 1977, underwater explorers discovered that there was in fact something, and quite a lot of it. At midocean ridges, where new ocean floor rises up as molten rock from Earth’s interior, where cold seawater mixes with the rising magma and, heated to 650 degrees, spews back up through chimney-shaped hydrothermal vents, researchers stumbled across bustling ecosystems. Clinging to the sides of the chimneys were thick white mats of bacteria; around them were eight-foot-long stalk-shaped worms, rocking in the water, while eyeless shrimp seethed around the chimneys like maggots. All were thriving on the energy bound up in the vents’ sulfur compounds. The seafloor might still be dark, but now it was known to be dotted with gardens.

In just the past eight years, however, underwater explorers have discovered that this picture is still incomplete: there is light at the bottom of the sea. Hydrothermal vents glow, and while the light is too faint to be perceived by the human eye, that hardly means it is without significance. Physicists maintain that although some of the light may be created by the intense heat, much of it must be attributed to some as-yet- unknown process. Biologists, meanwhile, say there is sufficient light at these vents for photosynthesis to take place. Researchers can’t say yet whether any creatures are actually living off this light, but if they are, they will represent the first known instance of natural photosynthesis without sunlight. The evolutionary implications may run deeper: it’s possible not only that this deep light is fueling photosynthesis now, but that, 3.8 billion years ago, it got the whole process started.

Behind the exploration of this phenomenon, and much of the speculation surrounding it, is a woman named Cindy Lee Van Dover. Van Dover’s pursuit of deep light began in 1986, when she was at Woods Hole Oceanographic Institution on Cape Cod, casting about for a Ph.D. project. Just a year earlier, explorers had discovered the first vents in the Atlantic, and they had scooped up some of the resident gray shrimp for biologists to study. Van Dover’s adviser, Fred Grassle, had gotten hold of some of the preserved specimens. I had just started as a grad student, and Fred said, ‘Here Cindy, you could use this as a project,’ Van Dover remembers. I was looking at their feeding biology, to figure out how they fit into the whole picture.

At first glance, the shrimp looked pretty much like their more common relatives living closer to the surface. The chief difference was that these shrimp had no eyestalks. That wasn’t surprising, given the darkness of their habitat--presumably the shrimp had lost their eyes because they were no longer necessary. Indeed, the explorers had named the shrimp Rimicaris exoculata, or eyeless fissure shrimp.

But when Van Dover looked over videotapes taken of the shrimp at the vents, she noticed that each animal had a strange pair of bright strips running along the front third of its back. She had missed them on her specimens because they had become dull during their preservation. Cutting open the shrimps’ backs, she found that the strips were in fact two flaps of tissue that joined and connected to a large nerve. They seemed to be some kind of sense organ. That’s when Van Dover had what she calls a silly idea: Could this organ, she wondered, be some kind of eye?

She got in touch with Steven Chamberlain, a neuroscientist at Syracuse University who specializes in invertebrate eyes. She called me cold and said, ‘I would like you to look at this and tell me if it’s an eye,’ recalls Chamberlain. She sent me the stuff, and at first I said, ‘Jesus, I don’t know if it’s an eye. Maybe.’ He put some of the tissue under a microscope to look at its fine structure. The tissue had broken down--most likely because the shrimp had been badly preserved--but nevertheless Chamberlain concluded that he was looking at mangled photoreceptors. I could imagine what it looked like before it got screwed up. If you destroyed an eye, this is what it would look like.

Van Dover turned next to Ete Szuts, a physiologist at Woods Hole who is an expert on pigment molecules. Szuts isolated pigment from the organ and tested it to determine which frequencies of light it absorbed. He found that its pattern of absorption was identical with that of a substance called rhodopsin--the pigment in the retinas of humans and other animals that captures light and makes it possible for us to see. Now Van Dover could only conclude that her silly idea was correct: the shrimp had eyes, albeit ones that had been radically reworked by evolution. They couldn’t form images, but their crowded photoreceptors suggested they were sensitive light detectors. Yet what could a shrimp be looking at if it was living in an endless night? She began to wonder if the vents weren’t quite as dark as people thought.

It was a possibility, if only barely. When water or rock is heated to the temperatures found around a hydrothermal vent, it will, like a heated toaster coil, radiate away some of that energy in the form of light. Most of this radiation will be at infrared wavelengths and thus invisible to all known living animals. But a little of it will turn up at the low end of the visible spectrum, and perhaps the shrimp were managing to gather this iota of light. It was hard to say how much might be available; the cold seawater surrounding the vent probably absorbed much of it, but no one had ever done the calculations on how much thermal radiation would be visible in such a bizarre environment. And certainly no one had ever noticed any light at these sites.

Van Dover needed someone to go down and look. She turned to geologist John Delaney of the University of Washington. Delaney, scheduled for a mission in the submersible Alvin, was planning to use a sensitive digital camera to survey the ocean floor around vents on the Juan de Fuca Ridge off the Washington State coast. Van Dover soon talked him into configuring the camera on one dive to look for vent light. And so in June 1988, after Delaney had plunged a mile and a half below the surface of the sea and positioned himself a foot and a half from the surging waters of the vent, he did something no vent visitor had ever done before: he turned out his lights. It was a dangerous maneuver because the vent smoke might have melted the camera or blackened Alvin’s windows. Van Dover was onboard the mother ship, Atlantis II, pacing the deck while Delaney pointed the camera at what looked to him like complete darkness. Then, as Alvin began an hour- long ascent, she received a short message from the bottom of the sea: vents glow. Delaney’s camera had captured a sharply defined glow along the vent, hovering in the darkness like the grin of the Cheshire cat.

Van Dover’s initial burst of luck got her into both the scientific and the popular press, but she is the first to admit that her work was far from airtight. Even after Delaney went on a second dive and put a series of filters in front of the lens, Van Dover had only a rough guess as to what kind of light the vent was producing. There were also questions about her shrimp. Finding some rhodopsin-like pigment and some structures that looked like photoreceptors was all well and good, but her case would have been far more solid if she had recorded the nerves responding to light or watched a shrimp use its light-gathering organ in the wild. Some skeptics suggested that the organs were likely nonfunctioning, vestigial eyes. Others went so far as to suggest that the structures might not be for vision at all but for listening to the raging vent water, or smelling the rotten-egg aroma of the sulfides it carries.

Getting closer to the truth, though, was hard. If, as Van Dover claimed, the shrimp had exquisitely sensitive light detectors, then even a moment in the glare of Alvin’s lights would leave them permanently blind. Watching how the shrimp move around naturally was thus out of the question. But Chamberlain had a feeling that if he could get his hands on more shrimp and preserve them properly, there might be more to learn. Anatomy is an art, he explains. If you take a Julia Child recipe and try to make a French quiche, you’re going to make a gooey mess the first time. The people who did the first samples had a good recipe, but they didn’t have the experience.

Chamberlain did. In 1993 he caught and preserved a new batch of shrimp, with the organs splendidly intact. Then, back at Syracuse, he and his colleagues were able to map out the structure of the shrimp’s alleged eyes, and everything they saw confirmed Van Dover’s inspired hunch. The organs turned out to be exquisitely designed for gathering scanty light, with oversize light-collecting photoreceptors taking up most of the available space. Shrimp have compound eyes, much like flies, with multiple lenses that focus light onto individual sets of photoreceptors. Most shrimp have shields of dark pigment cells between photoreceptors so that light won’t leak from one set to another and blur an image. In R. exoculata, however, the pigment cells are tucked underneath the eye, out of the way, allowing all photoreceptors a chance at the thin rain of photons. If Chamberlain had any doubt left that he was looking at eyes, it was dispelled when his group detected neurotransmitters--chemical messengers-- that other shrimp use nowhere but in their eyes. That to me is just the icing on the cake, Chamberlain says.

Chamberlain’s team has since discovered a second species of shrimp at the same Atlantic vent, with the same eyes. These smaller, orange animals also carry their eyes on their back, and Chamberlain thinks this position is critical to the survival of both species. The animals live on the sides of the chimneys, where they feed on mats of bacteria. Since the light pours out of the top of the chimney, the shrimp normally live in its shadow. If they move out of the shadow, the vent light falls on their backs. Registering a faint glow tells the shrimp that they are in the wrong place. They may simply be drifting away from the vent and out into open water, or they may be making a more serious mistake, moving up the side of the chimney until they get too close to its vent--in which case they may be swept away and instantly cooked.

Somebody needs to look at the visual structure of all the other animals at the vents, says Chamberlain. Nobody has ever done that because we just assumed they were blind. What about the fish, what about the crabs- -what do their eyes look like? We don’t know anything about any of that yet.

After her brief stint in the glow of the vent light, Cindy Van Dover’s life quickly became busy. The day after earning her Ph.D. in 1989, she joined the Alvin team, becoming the first woman pilot of the craft. For the next several years biological research in the deep sea kept her hurrying between the Atlantic and the Pacific. Not until 1993 did she manage to find enough time to take another look at the light.

By then she had learned that her original readings of the vent light, which Delaney had obtained by placing different filters in front of a camera, were woefully crude. The result was a bit like watching a movie and seeing only the reds for a few minutes, then only the blues, then only the yellows. Van Dover simply needed to see the light more clearly. Fortunately she was able to team up with someone who could give her a new set of eyes.

Alan Chave makes his living at Woods Hole as a marine physicist, but undersea explorers have come to rely on him for his talents as an inventor of unusual sensing equipment. After volunteering to help Van Dover, he quickly figured out that what she needed for seeing some of the dimmest light on Earth was essentially an industrial-strength photometer. He bored out a clear Lucite rod and placed four photodiodes inside that would emit current each time they were hit by photons. It’s tricky to build, simply because the currents in the photodiodes at that light aren’t a lot, says Chave. You’re close to a noise level for a decent amplifier. A little bit of stray current and you’ve killed yourself.

He dubbed his creation opus--Optical Properties Underwater Sensor. Like the shrimp eyes, opus couldn’t form an image, but it could gauge the intensity of the faint light. Best of all, Chave could put a filter in front of each photodiode so that it could measure light at four different frequency bands at once.

In 1993 and then again last spring, Van Dover and Chave took opus down on a total of a dozen dives. Each time they came to the surface, they didn’t know exactly what they had seen until they had taken opus to the Harvard-Smithsonian Observatory in Cambridge, Massachusetts. There they could calibrate its sensitivity with a device normally coupled with telescope cameras that capture the dim light of stars. With the help of Princeton physicist George Reynolds, they were then able to do the computations that allowed them to determine the number of photons coming from the mouth of the vent.

This haul of deep-sea data has been slow, but it has been worth the effort. As Van Dover and her colleagues reported this summer, the glow at the vents is no ordinary light. At some sites, for example, it is actually a sporadic flickering, which is not the kind of pattern that thermal radiation alone could produce. They have found that the vent light is much brighter at all frequencies than the spectrum Reynolds predicted for thermal radiation alone. At some wavelengths it was as much as 19 times stronger than predicted.

There certainly is thermal radiation, but there’s also something else out there, says Chave. Beyond that, I can’t tell you what it is right now. Candidates abound, and most are exotic--minerals may be cracking and emitting light, for example, or bubbles of gas may be imploding and the high pressures may be producing a glow. Chave is building a new camera that will be able to narrow the field of possibilities: unlike opus, this one will be able to see images. It will consist of one large digital camera chip with nine different lenses, each focused on a different sector of the chip and each set to gather a different frequency of light. When Chave takes his new camera on a dive next fall, he’ll essentially be able to take nine different movies of the vents with a camera so sensitive, he says, that it can just about measure a single photon.

Meanwhile, the implications of the opus results are more than enough to keep Van Dover excited. Up on land, on a sunny day, a tree is bathed by roughly a quintillion (a billion billion, or 1018) photons per square inch per second. But researchers have found that some organisms can photosynthesize with far less. Bacteria in the Black Sea hold the record: they eke out an existence at 240 feet below the surface, where they receive only about a trillion (1012) photons of sunlight per square inch each second. The deep vent light detected by opus is at about that same level. In other words, there is enough light for photosynthesis--of a completely nonsolar kind.

Thoughts of photosynthesis have floated through Van Dover’s mind ever since she first discovered hydrothermal light. When we came off the boat in 1988, I had a beer with a colleague of mine, and I said, ‘Hey, what if there’s enough light for photosynthesis?’ He just said, ‘What a stupid idea.’ But that was the big hook for me. What if there were?

If bacteria were photosynthesizing in vent light, they might simply be newcomers that had drifted down to the vents recently and adapted to the dim light, much like the shrimp. On the other hand, their pedigree could be much older. The heat-tolerant, sulfur-eating microbes around the vents are among the most primitive creatures on Earth, and some researchers have suggested that life itself originated around those rocky maws. To Van Dover, these were only musings that she sometimes threw out at conference talks for intellectual fun. During one talk in 1994, however, someone in her audience took her seriously.

Euan Nisbet, a paleontologist at the University of London, specializes in life during the first 2 billion years of Earth’s existence. When he heard Van Dover’s talk, he wondered if she might be pointing toward an explanation of the origin of photosynthesis. Photosynthesis is the kind of problem that goes back to Charles Darwin, says Nisbet. How do you construct something so complicated when it’s hard to understand the advantage of the intermediate steps?

Photosynthesis happens in plants and some species of bacteria when chlorophyll or another pigment molecule catches light and transfers the energy to a neighboring molecule, exciting one of its electrons. A third molecule then grabs the electron and passes it down a long line of other molecules, each of which sucks away a little energy, which it uses to power one of the many reactions needed to turn hydrogen and carbon dioxide into fuel for the organism.

Nisbet had the idea that photosynthesis might have begun as phototaxis--simple movement by an organism in response to stimulation by light. This notion comes back around to the elementary fact that when you live at a hydrothermal vent, it pays to know where you are. Bacteria don’t have eyes like shrimp to gauge their location, but that doesn’t necessarily mean they are blind. Many microbes can sense light. Some marsh dwellers, for example, move down through the sediments to the layer in which visible light is low but infrared light still penetrates; this happens to be the place where they find the most food.

Together, Nisbet and Van Dover hashed out the following scenario for the origin of photosynthesis: Imagine a hydrothermal vent on the early Earth. At first the microbes feeding on sulfides around the vent can’t sense their position, and sometimes they drift away into the cold and freeze; sometimes they get too close to the mouth of the chimney and fry. But some of the bacteria carry molecules that serendipitously absorb the light emitted by the vent. Gradually, descendants of these bacteria develop the ability to use the light to keep themselves in a safe place (or even to figure out where the most food is on the vents), and these bacteria thrive.

Some millions of years later, this story goes, a few of these phototaxis-capable bacteria drift up from the dark depths of the ocean to shallow hot springs, where they can continue on their old diet of sulfides. Now, though, they no longer live under a faint drizzle of light from vents but under a torrent of light coming from the sun. Thanks to their vent ancestry, they can already trap photons; all they have to do now is become sensitive to visible light and then find a way to harness this captured energy, by evolving a system of molecules that can convert the captured energy into fuel. Modern photosynthesis is born.

We’re simply suggesting a starting step, but in many cases the starting step is the hardest to imagine, says Nisbet. It starts as a heat-detection mechanism, you get organisms knocked out into shallow environments, and they happen to have the equipment onboard to detect sunlight. Now they have something that gets them a free lunch from the sunlight upstairs, and then there’s a whole new world up there. As for supporting evidence, he points out that the most primitive forms of bacterial chlorophyll absorb the most light at the frequency bands that Van Dover measured at hydrothermal vents. Moreover, photosynthesis today makes use of certain elements--iron, manganese, and sulfur, to name three--that are abundant around hydrothermal vents. It’s not proof, but it is neat. We’re simply saying that the facts are consistent with the hypothesis.

This spring Van Dover began searching for the telltale signs of photosynthesis at a vent site in the Atlantic called Hole-to-Hell. We nabbed the top of the chimney and came back up with a chunk of sulfide in a box, she says. Back at her lab at the University of Alaska, where she now works, Van Dover began to dissolve the rock. If she’s lucky, she’ll be able to find pigments in it, and if she does, she’ll look at the absorption pattern. Any chlorophyll will have a very characteristic absorption, she explains. If we find that, we can think about doing molecular work. The next step will be to gather more rock and try to extract fragments of bacterial dna.

In all honesty, Van Dover isn’t very optimistic about her latest hunt. I really don’t expect to find pigments. It seems like I’d be too lucky to find photosynthesis on the seafloor. But it would be like all the other things in the deep sea. We keep saying no to new ideas. We think the deep sea is cold, unchanging, and flat, but it’s not cold everywhere, it’s not unchanging, and it’s not flat. Shrimps have eyes? ‘No,’ we say, ‘shrimps can’t have eyes!’ But there’s light down there! So I figure I’ll press forward in my naïveté and see what I find.
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