Human-like 'eye' in single-celled plankton: Mitochondria, plastids evolved together

The single-cell marine plankton, a predatory microbe, bears a dark purple spot known as an ocelloid. It resembles the multicellular eye of animals so much that it was originally mistaken for part of an animal the warnowiids had eaten.

Canadian Institute for Advanced Research senior fellows Brian Leander and Patrick Keeling supervised lead author Greg Gavelis at the University of British Columbia and, in collaboration with senior fellow Curtis Suttle, showed that this eye-like structure contains a collection of sub-cellular organelles that look very much like the lens, cornea, iris and retina of multicellular eyes that can detect objects -- known as camera eyes -- that are found in humans and other larger animals.

The researchers gathered single cells of warnowiids off the coasts of B.C. and Japan, sequenced their genomes, and analyzed how the eyes are built using new methods in electron microscopy that allow the reconstruction of three dimensional structures at the subcellular level.

They found that a layer of interconnected mitochondria, organelles that supply energy to cells, surrounds a robust lens and makes up the warnowiids's equivalent of a cornea. In addition, a network of interconnected plastids that originated from an ancient symbiosis with red alga radiate from the retinal body.

Plastids have their own genome and are responsible for harvesting energy from light in photosynthetic plants and algae. The scientists determined that the retinal body contains a plastid genome suggesting components of the light-harvesting machinery may have been adapted to use in detecting light for sensory functions rather than to acquire energy.

Scientists still don't know exactly how warnowiids use the eye-like structure, but clues about the way they live have fuelled compelling speculation. warnowiids hunt other dinoflagellates, many of which are transparent. They have large nematocysts, which Leander describes as "little harpoons," for catching prey. And some have a piston -- a tentacle that can extend and retract very quickly -- with an unknown function that might be used for escape or feeding.

The team speculates that the eye-like structures help warnowiids detect their dinoflagellate prey and send chemical messages to communicate with other parts of the cell. Dinoflagellates have a uniquely large nucleus with tightly packed chromosomes that can change the polarization of light passing through them. One possibility could be that warnowiids can detect the light's orientation change as it passes through their transparent prey, showing them in which direction to hunt.

"The internal organization of the retinal body is reminiscent of the polarizing filters on the lenses of cameras and sunglasses," Leander says. "Hundreds of closely packed membranes lined up in parallel."

Definitive evidence for how ocelloids function remains elusive for now, because warnowiids are very hard to find and have never been grown in the lab. The team surmounted this problem by conducting their investigations on single cells isolated from nature. The work sheds shed new light on how very different organisms can evolve similar traits in response to their environments, a process known as convergent evolution. Eye-like structures have evolved independently many times in different kinds of animals and algae with varying abilities to detect the intensity of light, its direction, or objects.

"When we see such similar structural complexity at fundamentally different levels of organization in lineages that are very distantly related to each other, in this case warnowiids and animals, then you get a much deeper understanding of convergence," Leander says.

"The project was facilitated by combining the different expertise found in the labs of three CIFAR fellows and Tula Investigators," Leander says. These were the Suttle Lab centres on marine viruses, the Keeling Lab centres on comparative genomics, and the Leander Lab centres on evolutionary morphology. Keeling, Suttle and Leander are all part of the CIFAR program Integrated Microbial Biodiversity.

The research will be published in the July 9 print issue of Nature.