More than meets the eye: the development of a complex eye structure in Warnowiids

by JT

In the world of microbiology, it’s always the most outrageous microbes that get all the buzz. Prokaryotic microbes, like Escherichia coli are usually the first examples of microbiology that come to most people’s mind. When you think about eukaryotic microbiology, yeasts like Saccaromyces cerevisiae involved in brewing and baking are the model examples. Or some insane fungi that can grow in and out of a host – I’m looking at you, Cordyceps.

Then there are the microbes that just do some weird, but awesome stuff by themselves. Like the warnowiids.

Warno-what?

The warnowiids are a little bit like the cousin you hear about at family reunions – they’re always doing something cool, but you’re not quite sure how they’re doing it, and you never really see them either. So what makes warnowiids so cool? They’re unicellular eukaryotic microbes that are flagellate protists, and have developed a complex eye structure called the ocelloid.

The ocelloid isn’t like a simple eyespot that has photoreceptors and allows the cell to respond to light. Instead, the ocelloid is made of similar structures that are analogous to what you might see in a human eye, although the exact function of the ocelloid is unknown (Figure 1). The ocelloid has a lens called the hyalosome, a cornea, an iris-like region, and a segment full of pigments called the retinal body (1). The retinal body functions similarly to how the retina works in our eyes, and is thought to function as a light sensitive component of the structure (Figure 2).

Figure 1. Microscopy and Illustrations of theOcelloid. Light micrograph (left), illustration (middle), and electron micrograph (right) of the ocelloid. The parts of the ocelloid and their evolutionary origins are labeled on the illustration.   

Figure 2: Analogous structures of the ocelloid andhuman eye. The ocelloid (left) has structures that are similar in function to structures in the human eye (right). H is the hyalosome, C is the crystalline lens, and R in both illustrations is the retina or retinal body.   

So you’ve got a unicellular organism capable of developing a highly complex structure typically reserved for multicellular organisms, and not just any multicellular organisms. The ocelloid structure was observed to be similar to multicellular camera-type eyes that evolved independently in different cephalopods and vertebrates (2).

These discoveries bring up some important food for thought. What role does multicellularity really play in the development of specialized structures such as the eye, if a single celled microbe can develop an analogous structure in the ocelloid? How did this development even happen? Why favor a complex ocelloid over a simpler eyespot? What are the evolutionary forces that drove the warnowiids to adapt this structure?

However, answering these questions wasn’t so easy due to how warnowiids grow and where they grow. Warnowiids are unable to be cultivated in a lab, making it difficult to grow and keep these cells viable for experiments. So why not just find isolates in the environment and just use those instead? The other problem is that warnowiids are also rare in the wild. They are typically found on plankton in marine environments, but they are found with rates of only one or two cells isolated from plankton per year (1). One or two cells! You’d have better luck finding affordable college education at that rate. Despite these obstacles, a few studies have come out in the last ten years detailing the structure and function of the ocelloid, as well as its evolutionary history.

In one study, researchers used electron microscopy and tomography to investigate the structure of the ocelloid (1). Electron microscopy uses electrons and tomography uses an ion beam to obtain images of the ocelloid. The authors also used genomics, both isolated organelle and single cell genomics in order to study the makeup of the ocelloid. What built the structures of the ocelloid?

It turns out that the ocelloid might be derived from different organelles. Previously, the retinal body was reported to have thylakoid-like structures. Typically, thylakoids are found within chloroplasts, and usually are the site of the light dependent reactions of photosynthesis. By using electron microscopy, the researchers found that during cell development, the retinal body appeared to be derived from a plastid-like structure with double stacked thylakoids (1). Plastids are organelles that usually house pigments used in photosynthesis, so this discovery brings into question what the function of the retinal body is if it contains these light harvesting proteins.

The researchers also used electron microscopy to examine the lens of the ocelloid, the hyalosome. They found that the lens contained a sheet of individual mitochondria that were connected to the cytoplasmic mitochrondria nearby. With the discovery of both thylakoid-like structures and mitochondria present in the ocelloid, the authors concluded that the ocelloid was composed of different organelle components. Mitochondria, similar to plastids, are thought to have an endosymbiotic relationship with warnowiids.

The researchers suggested that the presence of these plastid-like structures with thylakoids might indicate the ancestor of warnowiids were photosynthetic, helping to possibly narrow down what the evolutionary path of warnowiids might have been. There is also the question of where these plastids were derived from in the first place. In dinoflagellates, which warnowiids are a part of, plastids are thought to originate from endosymbiosis with red algae (1). Coupled with the mitochondria sheets found in the lens, these conclusions suggest that the ocelloid incorporates different endosymbiotic organelles together in order to form this complex structure.

Whoa. So instead of undergoing cell differentiation or similar mechanisms by which our own multicellular eyes develop, the warnowiids instead create a hodgepodge of different organelles in the form of mitochondria and plastids to achieve complexity. In some ways, the warnowiids have adopted a “fake it ‘till you make it” mentality when it comes to producing a complex structure of their own analogous to a multicellular structure found in our eyes.

So we’ve elucidated what we think the structure looks like, what its composed of, but what does it actually do? In another study, the researchers sought to determine the function of the ocelloid by determining if the structure was photoreceptive (3). The researchers examined the ocelloid using electron microscopy in two different light conditions, in a light adapted state and a dark adapted state (3). They found that the retinal body in the light adapted state had thicker lamellae compared to the dark adapted state. That is, the total surface area of the retinal body became larger in the dark adapted state, suggesting that the ocelloid does play a role in responding to light and dark conditions as a larger surface area has more chance to gather light. The researchers also found that the hyalosome can also play a role in light sensitivity by concentrating dim light (3). With these conclusions, the researchers determined that the ocelloid does play a role in sensing light and functions as an ocular structure.

As we figure out methods to cultivate organisms that were previously only able to be isolated from the wild, more experiments can be done on warnowiids to further investigate the evolutionary path that these organisms took in order to develop the ocelloid structure. This is important in two ways. One, the fact that ocelloids developed not out of multicellularity, but instead, a chimeric combination of different organelles provides another way to how complexity can be achieved in organisms. Second, the evolutionary forces that drove warnowiids to develop ocelloids might serve as an example of driving forces for other evolutionarily mysterious structures found in different organisms.

Warnowiids might not be in the public eye (no pun intended) as much as yeast, or fungi, or even other protists, but their unique development of a complex structure without multicellularity provide insights on how evolution could have driven this process, as well as how different photoreceptive structures in organisms are made and what their function is. Due to the difficulties in obtaining warnowiids, not many experiments have been done on these unique organisms, but in the next couple of years, we might be seeing more of these guys as cultivation techniques improve.

Keep an eye on them.  

References:

1.         Gavelis GS, Hayakawa S, White Iii RA, Gojobori T, Suttle CA, Keeling PJ, Leander BS. 2015. Eye-like ocelloids are built from different endosymbiotically acquired components. Nature 523:204–207.

2.         Hoppenrath M, Bachvaroff TR, Handy SM, Delwiche CF, Leander BS. 2009. Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences. BMC Evol Biol 9:116.

3.         Hayakawa S, Takaku Y, Hwang JS, Horiguchi T, Suga H, Gehring W, Ikeo K, Gojobori T. 2015. Function and evolutionary origin of unicellular camera-type eye structure. PloS One 10:e0118415.