by Edith Widder
As it turns out, a lot of luciferins are endowed with antioxidant properties. In many cases, luciferins first evolved as scavengers of oxidants that are toxic to cells. Only later, with the evolution of specific luciferases, did these molecules become involved in light production. Interestingly, in bacterial bioluminescence, it appears that the enzyme rather than the substrate is the detoxifying agent, but in both cases the underlying principle is the same: Key elements of the bioluminescent chemistries originally evolved because they provided protection from oxidation.
In the case of bacteria, based on the Polish experiment described above, it seems that the next key evolutionary step involved producing dim light to protect against cell damage from UV light. For that light to then become bright enough to be visible required a whole different kind of selective advantage—one that may help ensure a reliable food source for the bacteria in a food-poor environment.
Although it has been said that you can’t polish a turd,*16 in the ocean you can. In fact, if you’re the right kind of bacteria, you can make it positively shine. My first acquaintance with this phenomenon was as a graduate student in Jim Case’s lab. My classmate Mike Latz was involved with an experiment that demonstrated the camouflage trick of counterillumination in a deep-sea shrimp. During the course of the experiment, the shrimp, which was being held in a specially designed light-measurement chamber, rather suddenly began putting out a very bright and prolonged light emission that was in no way related to the overhead light it was trying to match. Upon inspection, it was discovered that the shrimp had produced a brightly glowing fecal pellet. What I love about this story is that the record of that “event” actually got published in an article about counterillumination in the prestigious journal Science. In the context of the article, there was no good reason to include the event, except that I think it appealed to Dr. Case’s perverse sense of humor.
It turns out that a lot of marine fecal pellets glow because the bacteria that help decompose them are bioluminescent. The reason for this, according to the “bait hypothesis,” is that by glowing en masse (dans la merde), the bacteria make themselves easy targets for visual consumers. The bacteria are consumed along with the pellet, thereby gaining access to the food-rich environment of the consumer’s gut. This now puts them at a significant advantage over non-luminescent bacteria, because dark bacteria will be essentially invisible and therefore far more likely to sink into the depths, where food sources are limited. This was a pretty remarkable insight that Bruce Robison and others first put forth in an abstract*17 published way back in 1977 and others have expanded on since.
As pellets sink into the deep sea and away from the harmful UV radiation of sunlight, the selective advantage of bioluminescence for the part it plays in DNA repair vanishes. When an energy-demanding process is no longer useful, it usually disappears, because mutations that diminish that process will be selected for. However, in this case, another selective advantage came into play because it favored bioluminescence for a wholly different purpose: providing better access to nutrients. By glowing, the bacteria attract roving food buffets, which is to say, the stomach contents of their consumers, but this strategy works only if there are enough bacteria present to be visible.
And so another amazing adaptation evolved, called quorum sensing. This remarkable trick allows bacteria to communicate with one another and thereby coordinate their efforts to benefit their mutual survival. In the case of bioluminescence, it assures that the bacteria do not expend energy manufacturing their light-producing chemicals unless they are present in sufficient numbers to be visible. In order to get the equivalent of a head count, the cells produce a small signal molecule. When the concentration of this molecule reaches a certain threshold level, it triggers a change in gene expression and the cells start producing the chemicals they need to emit light. Although quorum sensing was first discovered in bioluminescent bacteria, later this method of communication among bacteria was found in a surprising variety of bacterial processes, including virulence, antibiotic production, and motility.
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Glowing poop is a concept with a lot of appeal.*18 For instance, it helps explain why the escas on anglerfish function as lures: because they mimic a common food source, morsels of glowing excrement. And there is good circumstantial evidence for the bait hypothesis. For example, gut content analyses of fish have revealed an abundance of luminous bacteria; it has been confirmed that luminous bacteria survive passage through fish guts; and laboratory experiments have demonstrated that zooplankton inoculated with glowing bacteria are more readily located and preyed upon by nocturnal fish.
If populating fecal pellets benefits the survival of bioluminescent bacteria, then it seems to me that populating marine snow might be similarly beneficial. But based on my observations, “snow shine” requires either mechanical or photic stimulation. I have sat in submersibles for long stretches with the lights out without seeing a hint of snow shine, until I flicked the submersible’s floodlights on and off.*19 When I did, the flashback could be anything from “Meh” to “Holy smokes!” but there’s always something. And while the shapes may vary, the kinetics are always the same. It ramps up to full brightness quickly, glows for many seconds, and then slowly fades to black. The first such response is always the best; subsequent flashbacks are generally dimmer.
Perhaps this requirement for stimulation serves as a means of energy conservation. You know the old question “If a tree falls in the forest and no one is around to hear it, does it make a sound?” When marine snow falls into the deep sea and there’s no one there to see it, does it glow? My guess is no. It needs to be stimulated, either mechanically or by light—perhaps from the bioluminescent flashlights displayed by so many deep-sea denizens. Unless there is someone there to see and consume it, the snow would remain dark until it encountered the bottom, resulting in the mechanical stimulus that would cause it to light up. Evidence that this may be the case has come to light from a very unexpected source: physics.
Shortly after I started my graduate studies with Jim Case, I answered the phone one day in the lab and found myself speaking with an overwrought physicist. He was part of a major neutrino detection*20 project that had placed a large array of ultrasensitive light detectors deep in the ocean, as far as possible out of the reach of sunlight. Their idea was to find the darkest place they could, and these detectors were intended to identify neutrinos by the dim flashes of light generated as charged particles streak through the water faster than the speed of light.*21
The trouble was that their detectors were seeing way more light than they should. The physicist called our lab because someone had suggested that the light might be bioluminescence. In a voice that was actually shaking, he asked, “Can this be true?” I assured him that it could. There was a long pause and then he asked, “Is there some place in the ocean where there isn’t any bioluminescence?” My answer—“Not that I know of”—did not make this man happy.
It may seem incomprehensible that this large, expensive project got funded with such a major flaw in the experimental design, but that is simply an indication of how little known the full extent of bioluminescence in the oceans was—and still is! That project, known as DUMAND (Deep Underwater Muon and Neutrino Detection), struggled for nearly two decades between 1976 and 1995, suffering an endless string of technical difficulties associated with trying to install an array of ultrasensitive light detectors 15,750 feet deep in the Pacific Ocean off the Big Island of Hawaii, before it was finally abandoned.
Another project with similar goals has since replaced it. Situated 8,200 feet deep in the Mediterranean Sea off the coast of France, this neutrino detector goes by the painfully contrived acronym Astronomy with a Neutrino Telescope and Abyss Environmental Research project, better known as the ANTARES telescope. This system, too, has had issues with bioluminescence that has impacted its detection limits and required some sophisticated background suppres
sion tricks, but not only does it work for detecting neutrinos, it has also resulted in the longest continuous time series of deep-sea bioluminescence ever recorded.
Several noteworthy observations have arisen as a result. The first is that, in an effort to better understand the bioluminescence they were observing, they did some sampling that provides—at minimum—circumstantial evidence that most of the bioluminescence they have recorded with the ANTARES telescope is the result of bioluminescent bacteria and that these bacteria are associated with particles rather than being free-living. The researchers also did tests on the impact of pressure on some of those bioluminescent bacteria and discovered that they emitted five times more light at high pressure than at low pressure—which suggests that they are uniquely adapted for life in the deep sea. And most intriguing of all, they found a linkage between seasonal periods of intense marine snow blizzards and increased bioluminescence recorded by the telescope.
The fact that a marine snow blizzard hitting the deep-sea floor may trigger a lot of bioluminescence could help explain how animals can visually locate food even in the three-quarters of the seafloor that appears devoid of life.
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Besides marine snow, another major source of food that accumulates on the deep-sea floor arrives in the form of dead creatures. These food packages are sometimes called deadfall or, for the largest of them, whale fall, and their size makes them a bonanza, for which there is stiff competition. Here, too, bioluminescence must come into play, as large food falls may be revealed not just by downstream scent trails, which are often highly directional, but by bioluminescence, which can be omnidirectional and visible over considerable distances.
The arrival of a food fall on the abyssal plane could be revealed by the mechanical stimulation of bioluminescent marine snow and plankton colliding with a carcass that protrudes into the bottom current. Or bioluminescent animals attracted to the bait may be stimulated to luminesce to defend themselves from other onsite predators. Or, if the bait becomes infected with bioluminescent bacteria, it may glow like a supersized fecal pellet. In any of these cases, large mobile predators with eyes, like giant sixgill sharks, would be at a distinct advantage. First come, first served.
The prevailing thinking on gigantism like that of sixgill sharks is that their size is advantageous because it permits greater energy storage, allowing long swims between food buffets. There has been some concern recently among deep-sea biologists that those swims must be growing longer thanks to the extreme impact of overfishing, which has greatly reduced the number of food falls reaching the deep-sea floor. However, there was still one more amazing finding that came out of our Deep Scope missions, which suggests that sixgill sharks have a feeding trick that may afford them an alternative energy source.
During our Deep Scope mission to the Bahamas in 2007, we saw sixgill sharks that were apparently drawn into the vicinity of the EITS camera either by the scent of the bait or by the visual stimulus of the e-jelly, but instead of going after the bait, these mammoth creatures oriented their bodies vertically in the water with their heads down as they sucked up sediment, then blew it out of their gills in billowing clouds. Our presumption was that they were feeding by sieving out burrowing creatures that inhabit the upper layers of soft sediment.
Although the vast, featureless regions of the deep-sea floor were once thought of as desertlike, we now know this not to be the case. In fact, an impressive assortment of small creatures like worms, crustaceans, gastropods, and nematodes burrow through and feed off the detritus that settles there and might well serve as a resource for these giants when food falls are scarce.
But before we could publish this remarkable finding, we needed to do a follow-up study, in which we planned to collect sediment samples at each deployment site so we could document that this was indeed a form of feeding. Unfortunately, we never got the chance. The 2009 expedition was my last mission with the Johnson-Sea-Link submersibles. In 2010 Harbor Branch retired them, sold off the last of its ships, and shortly thereafter laid off the crews. It seemed that the golden age of submersibles was coming to an end.
Skip Notes
*1 John Murray and Johan Hjort, The Depths of the Ocean (London: Macmillan, 1912).
*2 Middle school must have been hell.
*3 High school was probably no picnic, either.
*4 A thankfully short-lived punk rock dance craze.
*5 Paragorgia arborea.
*6 Mushroom coral, or Heteropolypus ritteri, formerly Anthomastus ritteri.
*7 Parazoanthidae.
*8 Lophelia.
*9 Alcyonacea.
*10 Actinoscyphia.
*11 That oh-so-valuable molecule green fluorescent protein (GFP), which has been used to greatly advance cell biology research by illuminating the inner workings of cells, was extracted from the jellyfish Aequorea victoria and is believed to be an adaptation to shift blue bioluminescence to green in this coastal species.
*12 In some species, the light organ actually rotates backward like the headlights on your Lamborghini.
*13 Not a table designed by Shakers, but an oscillating platform used to stir substances in a tube or flask.
*14 Preferably sunscreen without the coral-damaging chemicals oxybenzone and octinoxate.
*15 You can actually purchase these powered-by-light enzymes in some “age-defying” skin care products…for only half the price of beluga caviar.
*16 Often used in reference to junk cars—like the VW bug that David and I rebuilt out of spare parts.
*17 A scientific abstract is a short overview of a scientific paper or presentation. This was a summary of a presentation made at the Western Society of Naturalists.
*18 Just imagine the possibilities in the novelty item industry alone.
*19 Two short pulses of light work better than one.
*20 Neutrinos are created by radioactive decay, including that which occurs in the core of a star, making their detection useful for a branch of astronomy known as neutrino astronomy, which allows astronomers to explore the cosmos with new eyes.
*21 Although nothing can travel faster than the speed of light through a vacuum, some particles can travel faster than the speed of light through water, and when they do, they generate light called Cherenkov radiation, named after the Russian scientist who first demonstrated it. Just as an aircraft traveling faster than the speed of sound through air emits a sonic boom, a particle traveling faster than the speed of light through water emits a kind of light boom. Cherenkov radiation is the cause of the blue glow associated with underwater nuclear reactors.
Chapter 13
THE KRAKEN REVEALED
KABOOM! It was a deafening crack, not something you want to hear on a ship far from shore. The lights went out, and I bolted for the fantail along with the other scientists who had been crowded around the laptop excitedly viewing the video we had just downloaded. As soon as we stepped on deck, it was clear the ship had been hit by lightning. Bits of the ship’s antenna were all over the deck, and a pillar of yellow and brown smoke was drifting aft. Never in all our considerable cumulative seagoing experience had any of us been on a ship that was hit by lightning. As we were remarking on that fact, we all seemed to have the same thought at the same moment: Crap! We didn’t back up the video! Did the computer get zapped? To have possibly lost the first footage ever recorded of a live giant squid in U.S. waters was a horrifying thought.
Among marine biologists, the giant squid often serves as a symbol, much like Captain Ahab’s great white whale, for “the one that got away.” Jokes and references to giant squid are just part of the seagoing culture. The tension on a trawl line suddenly increases and somebody will say, “Must have caught a giant squid.” A net comes up
empty and shredded and the giant squid gets blamed. To claim to have filmed a giant squid and then have to say “You’ll just have to take our word for it” would never cut it.
For some marine biologists who have spent their careers hunting the giant squid with Ahab’s fervor, the opportunity to be the first to see the world’s most famous invertebrate in its natural habitat was the goal of a lifetime. For others, like me, it was merely a highly improbable fantasy.
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Ancient mariners told many tales of terrifying sea monsters whose size and ferocity grew with every flagon of spirits consumed during the storytelling. One of the most famous of these leviathans was known to Norwegians as the Kraken, a titan that struck terror in the hearts of seafarers. They described it as a multiarmed beast so enormous it could be mistaken for an island when seen floating at the surface, and so deadly it could drag men and ships to watery graves. We now recognize their accounts as providing a fair description of what we know as the giant squid, which goes by the scientific name Architeuthis.
There was much scientific skepticism of these early accounts, but proof finally came in 1861 when a French warship operating off the Canary Islands happened upon one of these behemoths. It was apparently dying, but, not wishing to take any chances, the sailors fired some shots to finish it off before using a rope to try to haul it on board. The enormous weight of the beast caused the line to slice through its body, with the result that the multiarmed head end fell back into the sea.
