Single-Celled Creature Has Eye Made of Domesticated Microbes

The oceans are full of eyes. Giant squid scan the depths with the world’s largest ones, which are oddly similar to those of the sperm whales that hunt them. Mantis shrimps watch for prey using eyes that work like satellites. Starfish stare through the tips of their arms, chitons look up through lenses made of rock, and scallops peer at the water through dozens of eyes with mirrors inside them. But to see the strangest eyes of all—eyes so weird that we can’t even be sure that they are eyes—you have to squint.

These maybe-eyes belong to a group of rare, free-swimming algae called warnowiids. Each consists of a just one round cell, so small that a few hundred of which could fit in this full stop. Under the microscope, each warnowiid contains a conspicuous dark dot. This is the ocelloid. It consists of a clear sphere sitting in front of a dark red strip, and has components that resemble a lens, an iris, a cornea, and a retina.

Eyes are meant to be animal inventions. They’re supposed to comprise many cells. They are icons of biological complexity. And yet, here’s a non-animal that packs similar components into its single cell. Is the ocelloid actually an eye? Can it sense light? What does a warnowiid use it for? These questions are still mysteries, but in trying to answer them, Gregory Gavelis from the University of British Columbia has discovered something about the ocelloid that’s even weirder. At least two of its components—the “retina” and the “cornea”—seem to be made from domesticated bacteria.

The first scientist to notice the ocelloids was a German zoologist named Oscar Hertwig. In 1884, while working at a research station in Naples, he was distracted by a tiny speck in a Petri dish. It appeared to be jumping up and down in the water as if crying for attention. Hertwig sucked it up with a straw and stuck it in ethanol—which was a mistake. The creature started to disintegrate, and Hertwig speed-drew it as quickly as he could, until it had completely broken down. He then published his observations, describing what looks like an eye.

Karl Vogt, a more senior zoologist, wasn’t having any of it. He accused Hertwig’s of grossly misinterpreting a horribly distorted specimen. A single cell couldn’t possibly have an eye; instead, the creature must have just scavenged an eye from a dead jellyfish—and yes, some jellyfish have eyes. The debate raged back and forth until Hertwig, who never found a second warnowiid to study, moved on to other things (and great acclaim).

No one saw the creatures again until 1921, when Charles Atwood Kofoid and Olive Swezy showed that they live all over the Pacific coast of North America. They were rare, though, and many of the species that Kofoid and Swezy drew have never been seen since. This rarity makes warnowiids extremely hard to study. You can’t culture them. You can barely find them. “You’d be lucky if you ever saw more than five in a single Petri dish,” says Gavelis.

You can, however, study their genes. Sequencing technology has progressed to the point where scientists can parse the DNA of a single cell. Gavelis’s team, led by Brian Leander, used these techniques to study the “eyes” of two warnowiids—Erythropsidinium (the species that Hertwig drew) and Warnowia. In particular, he focused on a curved red structure called the retinal body, so named because it seems analogous to our light-detecting retinas.

Gavelis found evidence to support an old idea that the retinal body is a plastid—a type of compartment found inside the cells of plants and algae. The green chloroplasts that allow these organisms to make their own food, by harnessing the sun’s energy, are a type of plastid. They evolved from a free-living bacterium that was engulfed by an ancient cell and forced into servitude. Over time, this bacterium became an inextricable part of its host, and turned into the plastids we see today.

Cells can acquire plastids by engulfing and taming their own bacteria. Alternatively, they can steal someone else’s. The ancestor of the dinoflagellates—the group of algae that warnowiids belong to—did exactly this. It swallowed another red alga and claimed its plastids for its own.

In warnowiids, Gavelis thinks those pilfered plastids make up the retinal body. He dissected out these structures from the main ocelloids and amplified the DNA within them. Among these sequences, he found several active genes that are involved in photosynthesis and are only used in algal plastids. And when he repeated the same technique on entire cells, including the huge amount of DNA in the warnowiids’ main genomes, he found a far smaller proportion of photosynthesis genes.

Down the microscope, the team saw that the retinal body has physical features that are characteristic of plastids. Weirder still, it seems to sit within a network of interconnected plastids that look different, but are enveloped by a single membranous web. There could be just one plastid, or dozens of them. “They’re like drops of oil in a lava lamp,” says Gavelis. “The degree of specialisation in this one structure just boggled my mind.”

Gavelis also showed that the “cornea” of the ocelloid consists of little bean-shaped structures called mitochondria. Mitochondria also descend from free-living bacteria that were domesticated by ancient cells, in an extremely unlikely event that may have given rise to all complex life. For a few billion years, they have provided complex cells with power. In the warnowiids, they also… well, it’s not clear what they do. A continuous layer of them surrounds the “lens”, and seem to send small protrusions into it. They could be helping to collect light in the style of a true cornea, or they could be supplying the lens with energy.

That’s the biggest mystery about the ocelloid: what does it do? It certainly looks like an eye. It has components that would seem to focus light onto the retinal body. But for the retinal body to then respond to that light, it needs some kind of light-sensitive pigment. Chlorophyll is a possibility; the thing’s a plastid, after all. Gavelis’ team are also looking for traces of opsins—the proteins that are universally found in all animal eyes, from starfish to giant squid.

Even if the ocelloid is an eye, what could it possibly see? Fernando Gómez of the University of São Paulo recently told New Scientist that they help warnowiids to aim harpoon-like stings at their prey (he compared them to “snipers”). But Gavelis is sceptical. With just one ocelloid, each warnowiid has at most a one-pixel view of the world. “There were only so many things that it could do with such limiting processing power,” he says. “Even resolving an outline or a shadow is way beyond what anyone has demonstrated that a cell can do.”

Alternatively, the warnowiids could just be using their ocelloids to sense absolute light levels, so they can swim towards bright areas or keep in shade. But Gavelis isn’t happy with that idea either. Other dinoflagellates can sense light levels using much simpler eyespots, which have no lenses. The warnowiids must surely be putting their more complex structures to more complex uses.

Gavelis’ favoured idea is that they are looking for their prey: other dinoflagellates. These creatures reflect a particular kind of light called circularly polarised light, which could betray their presence. Perhaps the warnowiids use the ocelloids to detect this tell-tale signal, and swim towards the creatures that emit it.

Tom Cronin, a vision scientist at the University of Maryland, Baltimore County, is not convinced. “It’s a monstrous stretch,” he says. For a start, many other dinoflagellates eat their own kind and do so without complex ocelloids. Also, complex eyes don’t necessarily imply complex behaviour. The simple box jellyfish has 24 eyes, eight of which are surprisingly similar to our own camera-type peepers. “They have outstanding optics,” says Cronin, “but they’re primarily useful for orienting the animal, or for detecting edges of shadowed areas.”

Finally, he wonders if the ocelloid isn’t really an eye, but more of a “glorified chloroplast”. Maybe its function is to provide its owner with energy, and the “lens” is just a way of focusing more light? Maybe the eye-like elements help the creature to orient itself in the brightest direction?

“That’s inconsistent with the evolutionary history of these critters,” counters Gavelis. The earliest members of the group almost certainly made all of their own food through photosynthesis, but later members are almost totally predatory—and they’re the ones with the most complex ocelloids. Given that, the hunting hypothesis is looking good.

Solving this mystery will be hard, given how hard the warnowiids are to find and study. Cronin says, “In the end, we know more about the structure of the strange eye-like ocelloids, but their function is just as obscure as ever!”

Reference: Gavelis, Hayakawa, White, Gojobori, Suttle, Keeling & Leander. 2015. Eye-like ocelloids are built from different endosymbiotically acquired components. Nature http://dx.doi.org/10.1038/nature14593