When you look at the phytoplankton under the microscope you rarely would expect anything to look at you back. However, that might be a case if you caught a dinoflagellate from Warnowiaceae family with your plankton net! They possess a very unique eye (ocelloid) that has retina (photoreceptor) and lens-like structures being very similar to the multicellular eye.
Hayakawa et al (2015) performed a range of experiments with Erythropsidinium sp., aiming to understand the evolutionary nature and function of the ocelloid. Using the mix of transcriptomics and transmission electron microscopy methods, researchers confirmed the camera-type eye structure and showed the presence of the rhodopsin-like gene that is upregulated only within the ocelloid (achieved by in-situ hybridization).
The phylogenetic analysis of the rhodopsin-like sequence revealed its relation to Bacteria and Archaea where bacteriorhodopsin is commonly found. Therefore, this study provides an evidence for an endosymbiotic origin of the structure. Transferring of the cassette of only six genes might result in the presence of bacteriorhodopsin (Munn 2011, p64), therefore, such result is also a strong indicator of the horizontal gene transfer.
This work also gives a good justification of the evolutionary benefit of this particular close-to-the-multicellular-eye structure: by performing various experiments with light and assessing the result with microscopy, it was revealed that this special structure expands the light sensitivity ranges, adjusting the proton pump for the dim light and protecting the ‘eye’ from the light damage.
The phylogenetic analysis of the rhodopsin-like sequence revealed its relation to Bacteria and Archaea where bacteriorhodopsin is commonly found. Therefore, this study provides an evidence for an endosymbiotic origin of the structure. Transferring of the cassette of only six genes might result in the presence of bacteriorhodopsin (Munn 2011, p64), therefore, such result is also a strong indicator of the horizontal gene transfer.
This work also gives a good justification of the evolutionary benefit of this particular close-to-the-multicellular-eye structure: by performing various experiments with light and assessing the result with microscopy, it was revealed that this special structure expands the light sensitivity ranges, adjusting the proton pump for the dim light and protecting the ‘eye’ from the light damage.
However, the paper does not give any clue to the origin of the ocelloid parts and raises a question of how such structures as retina and lens could have evolved in bacteria? Or in dinoflagellate, after the endosymbiosis occurred?
A well-justified answer to those questions has been given by Gavelis et al. (2015). They looked at the three-dimensional structure of the retina in the Nematodinium sp. using focused ion beam scanning electron microscopy and organelle genomics.
They found that ocelloid in Nematodinium sp. has an autofluorescent pigment and, after observing the cell division process, came up with the suggestion that ocelloid might take its origin from the cell structures such as chloroplasts and mitochondria. Moreover, they found an evidence of the network between the retina and other organelles by using FIB-SEM tomography.
Another supporting evidence: researchers compared genes from the DNA that present in plastids with those found on the retina bodies and found out that the amount of plastid DNA in the retina was 1,600-fold higher than in the whole cell!
Such findings reveal a previously unknown complexity inside the cell and give a very well tested suggestion on why the ocelloid possess a very particular structure.
Another supporting evidence: researchers compared genes from the DNA that present in plastids with those found on the retina bodies and found out that the amount of plastid DNA in the retina was 1,600-fold higher than in the whole cell!
Such findings reveal a previously unknown complexity inside the cell and give a very well tested suggestion on why the ocelloid possess a very particular structure.
After reading both papers, it is hard to drive a solid conclusion on how the ocelloid evolved, however, one of the options might be a combination of both theories: it did occur in the cell as a result of an endosymbiosis but then was highly modified by interaction with other plastids. Such hypothesis can also be supported by the fact that other, less complicated, types of eyes exist in dinoflagellates.
Both papers provide a well-described idea of the origin of ocelloid, however, the research done by Gavelis et al. (2015) used more advanced and in-depth techniques, such as plastid genomics.
Both papers provide a well-described idea of the origin of ocelloid, however, the research done by Gavelis et al. (2015) used more advanced and in-depth techniques, such as plastid genomics.
An interesting further step would be to perform this method with Erythropsidinium sp. and test the Nematodinium sp. for the presence of the rhodopsin-like gene.
Paper reviewed:
Hayakawa, S., Takaku, Y., Hwang, J., Horiguchi, T., Suga, H., Gehring, W., Ikeo, K. and Gojobori, T. (2015). Function and Evolutionary Origin of Unicellular Camera-Type Eye Structure. PLoS ONE, 10(3), p.e0118415.
Hayakawa, S., Takaku, Y., Hwang, J., Horiguchi, T., Suga, H., Gehring, W., Ikeo, K. and Gojobori, T. (2015). Function and Evolutionary Origin of Unicellular Camera-Type Eye Structure. PLoS ONE, 10(3), p.e0118415.
Further reading:
Gavelis, G., Hayakawa, S., White III, R., Gojobori, T., Suttle, C., Keeling, P. and Leander, B. (2015). Eye-like ocelloids are built from different endosymbiotically acquired components. Nature, 523(7559), pp.204-207.
Gavelis, G., Hayakawa, S., White III, R., Gojobori, T., Suttle, C., Keeling, P. and Leander, B. (2015). Eye-like ocelloids are built from different endosymbiotically acquired components. Nature, 523(7559), pp.204-207.
Hello Anastasiia,
ReplyDeleteI really enjoyed reading this, and I think these organisms raise some very interesting questions about the evolution of vision. I was wondering if the authors mentioned any ecological implications of the dinoflagellate ocelloid, and photoreception in microalgae. The first one I could personally think of is the ability to exploit the ideal light intensity for photosynthesis. However the link to photosynthesis might not be this straightforward, as there appear to be both phototactic and photophobic behaviours in photosensitive microalgae: did the authors mention which photomobility behaviour Erythropsidinium sp. exhibits?
Thank you,
Alessandro
P.S.: I came across a very interesting article on the evolution of photosensitive structures and organs. Despite it being very animal-centric, you might find it interesting too:
Gehring, W. J. (2004) "Historical perspective on the development and evolution of eyes and photoreceptors". Int. J. Dev. Biol., 48. pp 707-717. doi: 10.1387/ijdb.041900wg
Hi Alessandro,
ReplyDeleteThank you for you question!
You are absolutely right, both papers refer to ocelloid's function as for being able to respond to the changing light intensity and exhibit areas with a better one. This particular structure described in the review, the camera type eye, is also thought to maximize the use of the dim light by adjusting the retinal body in order to get enough protons as well as protect the 'eye' from the light damage from bright light!
Thank you for the reference, I found the origin of photoreception bit particularly interesting. Again, that contradiction appears of whether it involved inside or outside the host!
Hello Anatasiia,
DeleteThank you for your reply. Maximising the use of dim light seems like an important feature of the camera type eye: it is evident that this structure has more complex implications than simply allowing phototactic behaviour. Its presence in a unicellular organism is truly remarkable.
Best,
Alessandro