Unicellular algae built compound eye of chloroplasts and mitochondria

Fig. 1. Comparison of microbial eye. a – dinoflagellates family Warnowiidae, b – chlamydomonas, c – fungal spores Blastocladiella. Notes in the text. Figure out the synopsis to the discussion paper in Nature.

Make a chamber eye having a cornea, iris, lens and retina, and can be a single cell component. To this end, representatives of the dinoflagellate family Warnowiidae use complex manner combined organelles – mitochondria, endoplasmic reticulum and chloroplasts former, lost the ability to photosynthesize.

Eye – is a classic example of a complex organ consisting of different tissues, which brings the body to benefit as a whole. Even Darwin asked questions about how animal compound eye could be formed gradually in the course of evolution. What Darwin replied that complex organs could well be formed gradually, because even imperfect eyes can give the body a slight advantage. For example, the light-sensitive cells, without additional devices may only help to determine the general direction of light. But this is better than total blindness.

Interestingly, a classic example of a complex organ like the eye chamber, may develop even in unicellular organisms. These eyes with all the necessary components – the cornea, iris, lens and retina – have representatives of plankton – dinoflagellates family Warnowiidae.

Single-celled creatures with complex eyes in the cytoplasm of cells have been described in the early twenties of the last century (see. Charles Atwood Kofoid & Olive Swezy, 1921. The free-living unarmored dinoflagellata). Then the researchers and had no idea that such complex eyes belong to microbes. It was therefore decided that the eyes in the cytoplasm – is nedoperevarennye remnants of jellyfish that feeds on plankton. Such a hypothesis long persisted because the representatives of dinoflagellates family Warnowiidae very rare. Furthermore, until now not chosen conditions for cultivating these microorganisms in a laboratory, which is why they and nowadays difficult to study.

Fortunately, over the past hundred years the arsenal of biological methods has expanded dramatically. Now, scientists can learn a lot of useful information even from just some few cells. For single cells is now possible to analyze the DNA sequence, gene expression levels, and even some amount of proteins. Only with the development of sensitive and accurate genetic methods scientists have carefully demonstrated that the compound eyes of dinoflagellates – it is their own development, rather than the remains of the victims.

An international team of researchers gathered a few dozen cells dinoflagellates family Warnowiidae off the coast of Japan and Canada. Scientists have identified the individual components of bacterial eye and analyzed the composition of nucleic acids. It turned out that the “retina” eye dinoflagellates is part of a complex system of chloroplasts, which stopped working in the specialty (dinoflagellates family Warnowiidae long ago lost the ability to photosynthesize). Nevertheless, in the old memory are continued to operate several specific genes of chloroplasts.

Even if the microorganisms found a structure very similar to the compound eye, which guarantees that it reacts to light? Studies show that reacts. Firstly, it was recently shown that the morphology of the “retina” eye dinoflagellates family Warnowiidae light-dependent (see .: S. Hayakawa et al., 2015. Function and Evolutionary Origin of Unicellular Camera-Type Eye Structure). Under the influence of light inner membrane vesicles of organelles became more elongated and flat. In the same article in the “retina” of these dinoflagellates we found gene expression of rhodopsin-like bacteria. The proteins in this group allow to feel the direction of the light and other microorganisms that have simple eyes – such as Chlamydomonas and fungus Blastocladiella, floating spores which also provided with photosensitive sensors. But there are other mechanisms of perception of the world: for example, using a light-sensitive protein euglena adenylate cyclase activated by light.

All microorganisms having eyes, these organs are arranged differently. In Chlamydomonas, like dinoflagellates family Warnowiidae, reacts to light part of the chloroplast (chloroplast only they work). The photosensitive spot on the edge of the chloroplast of Chlamydomonas contain rhodopsin, which partially shield the granules with the pigments carotenoids (Fig. 1). Screening photosensitive sensors with at least one hand it is necessary that the body could determine the direction of light. Others have “sighted” microorganisms – Euglena – eye is not related to the chloroplasts. In Euglena photosensitive proteins embedded in the membranes of special thick stack at the base of the flagellum. The direction of light provide granules with a pigment gematohromom. The spores of the fungus Blastocladiella device photosensor similar – rhodopsins membrane organelles located in the neighborhood with the flagellum, and near them are lipid vesicles, also likely to provide direction of the light incident on the photosensitive organelles.

Interestingly, the plastids, on the basis of which have different single-celled independently developed “eyes” have different origins: so, dinoflagellates Warnowiidae and Cryptophyta algae Guillardia secondary plastids (descended from symbiotic red algae – a representative of the eukaryotes), and in Chlamydomonas – primary, from symbiotic cyanobacteria. This is another argument in favor of the “eyes” on the basis of plastids developed in unicellular eukaryotes, many times independently. Among the many examples of unicellular generally convergent eye development of various “scrap” materials (often plastids, but not always, often using rhodopsin, but do not always).

All microbial eyes, investigated before, found only some simplified analogues of the retina (the membrane with proteins respond to light and the pigment granules, replacing a pigmented retinal cells of a multicellular eyes). A family Warnowiidae dinoflagellates have not stopped, and added to their eye still lens consisting of membranes of the endoplasmic reticulum, the focusing light on “retina” (Fig. 2). The lens significantly improves the image sharpness. Also dinoflagellates appeared shell eyes – the cornea, which consists, as scientists have found, from a plurality of connected into a single system of mitochondria. It turns out interesting and rather rare example of convergence in the two levels of life – unicellular and multicellular. Interestingly, in the creation of the compound eye of the microorganism involved, and both types of endosymbionts (mitochondria and chloroplasts), and his own membrane (endoplasmic reticulum).

Dinoflagellates family Warnowiidae feed on other plankton representatives, including other dinoflagellates. Scientists suggest that the eye helps them to monitor the movements of their victims, which Warnowiidae can hunt using cell “harpoons” – nematocysts. Some of dinoflagellates, which feed Warnowiidae, fluoresce. Therefore, they can be quite clearly seen only need to have an eye. So it is quite possible that we will soon know the answer to the question whether they see each other microbes.

Another notable feature of dinoflagellates – is constantly condensed chromosomes, polarizing light. Does the compound eye Warnowiidae distinguish polarized light, yet to be verified. But the internal structure of their “retina” with hundreds of parallel oriented membrane vesicles really similar to the polarizers, which are used, for example, in the sunglasses and the lenses of cameras.

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