Going green: the evolution of photosynthetic eukaryotes Saul Purton The chloroplast Look around our macroscopic world and evolutionary time. Ultimately, the once autonomous is the site of Gyou see a rich diversity of photosynthetic cyanobacterium became an integral and essential photosynthesis eukaryotes. A fantastic range of plants covers component of the eukaryotic cell – the chloroplast (see in plant and algal our land and numerous different macroalgae (seaweeds) Figs 1 and 2). This first truly photosynthetic eukaryote abound in our seas. Similarly, the microscopic world is almost certainly the common ancestor of three major cells. Saul Purton is filled with a wealth of exotic microalgae. However, photosynthetic groups found today: the chlorophytes explains how this all of these organisms share a common legacy – the (green algae and all plants), the rhodophytes (red algae) important organelle chlorophyll-containing plastid (=chloroplast) that is and the glaucophytes. The divergent evolution of these evolved from a the site of photosynthesis. This organelle has its three groups from the common ancestor has resulted in photosynthetic ancestral origins as a free-living photosynthetic chloroplasts with different pigment composition and bacterium. bacterium that became entrapped inside a primitive ultrastructure. The chlorophytes have lost the phyco- eukaryotic cell. The bacterium was retained rather bilins, but retained chlorophyll a and b, whereas the red than digested as food and a symbiosis was established algae and glaucophytes have chlorophyll a only, together in which the host cell provided a protected and nutrient- with phycobilins. Interestingly, the glaucophytes rich niche in return for the photosynthetic products have also retained the cell wall of the bacterium and generated by the bacterium. The story of how this their chloroplasts are bounded by an inner membrane bacterial endosymbiont evolved into a chloroplast and derived from the bacterial cell, a cell wall of peptido- was then spread by subsequent symbiotic events to glycans and an outer membrane derived from the food other eukaryotes is a fascinating and on-going one vacuole of the eukaryote. In the chlorophytes and that involves the study of a wide range of microbial rhodophytes, the cell wall has been lost and two eukaryotes. membranes surround the chloroplast. Coloured slaves Centralization of power Early in the history of eukaryotic evolution a simple Although the cyanobacterium escaped death by rule applied. Photosynthetic bacteria were the primary digestion, it was to pay a high price for its survival as a producers, utilizing the sun’s energy to convert carbon component of the eukaryotic cell. The several thousand dioxide to complex carbohydrates, and single-cell genes the bacterium brought with it, and which allowed eukaryotes were the consumers, often acquiring their Phagotrophic eukaryote food by engulfing and digesting the bacteria or other symbiosisPrimary Secondary symbiosis eukaryotes. The cyanobacteria (also called blue-green algae) were particularly important producers since Cyanobacterium they carried out oxygenic photosynthesis in which the harvesting of light energy is coupled to the Nucleus production of molecular oxygen from water. These Green algae early cyanobacteria probably contained several different Red algae light-absorbing pigments, including chlorophylls a and Glaucophytes b and phycobilins, and could carry out photosynthesis using a wide range of light levels and wavelengths. Importantly, the cyanobacteria would still be able to photosynthesize even after being incarcerated within the colourless cell of a phagotrophic eukaryote. The normal fate of the captured bacterial cell would be death by digestion. However, for the eukaryote a continuous supply of fixed carbon and oxygen was Chlorarachniophytes perhaps an attractive alternative to a quick meal, and Cryptophytes occasionally the death sentence would be commuted to life imprisonment. Under this arrangement, the RIGHT: bacterium would be allowed to grow and divide within Nucleomorph Fig. 1. The endosymbiotic its prison cell, and would therefore be retained and origin of chloroplasts. Note that the Dinoflagellates chloroplasts of euglenophytes and inherited by the eukaryote as it itself divided. Indeed, Heterokonts dinoflagellates actually have three examples of such endosymbiotic associations are Haptophytes membranes rather than four. It is found amongst modern-day eukaryotes. For example, Euglenophytes thought this reflects an alternative feeding mechanism in which the the cyanobacterium Nostoc survives inside the cells of cell membrane of the prey alga is the filamentous fungus Geosiphon pyriforme. discarded. In one particular case, the interdependence between Loss of Loss of the Chloroplast replacement photosynthesis chloroplast by further symbioses COURTESY S.PURTON the master and his slave became closer and closer over 126 MICROBIOLOGYTODAY VOL 29/AUG 02 for food because they could synthesize it ‘in house’ LEFT: from simple precursors using the power of photo- Fig. 2. Transmission electron micrographs showing the similarity synthesis. However, this meant that the algae also in ultrastructure between (a) a became targets for any hungry phagotrophic eukaryote. modern-day cyanobacterium As with the cyanobacterial prey, the engulfed algal (Pseudanabaena) and (b) the plant cells provided new opportunities for the establishment chloroplast (in this case in a of symbioses, although in this case it was a eukaryote tobacco leaf) that evolved from the cyanobacterial endosymbiont. that was being enslaved within a eukaryote (a process PHOTOS DR KARI LOUNATMAA (a) AND termed secondary endosymbiosis; see Fig. 1). Once DR JEREMY BURGESS (b)/SCIENCE again, the endosymbiosis occasionally led to a permanent PHOTO LIBRARY association between the two organisms and the evolution of the captured alga into a bona fide organelle. And BELOW: Fig. 3. Light micrographs once again the price for survival of the endosymbiont of various microbial eukaryotes was high. Since the only important part of the alga was that possess chloroplasts. (a) its chloroplast, other cellular components were rapidly A glaucophyte (Glaucocystis), (b) discarded. Consequently, the algal cell was reduced to the red alga Porphyridium, (c) Euglena, a euglenoid alga that it to live an autonomous existence, were unceremon- a chloroplast surrounded by additional membranes obtained its chloroplast from iously stripped from it leaving only a meagre genome of derived from the algal cell membrane and the vacuolar a green alga and (d) the a few hundred genes. Genes no longer necessary for an membrane of the phagotroph. Remarkably, the nuclear dinoflagellate Ceratium that intracellular existence (for example, those required for genes for the biogenesis of the chloroplast were once obtained its chloroplast motility) were simply discarded. Others were eliminated again moved en masse, this time from the algal nucleus from a red alga. PHOTOS MICHAEL ABBEY (a), ASTRID by a process of gene substitution in which nuclear to that of the new eukaryote host. & HANNS-FRIEDER MICHLER (b), ERIC eukaryotic genes functionally replaced their bacterial Various different algal groups appear to have evolved GRAVE (c) AND LEPUS (d)/SCIENCE counterparts. Finally, and perhaps most remarkably, via this process and include the dinoflagellates, the PHOTO LIBRARY there was a mass transfer of most of the remaining genes euglenophytes, the heterokonts (which include the from the bacterial genome to the eukaryotic nucleus. The diatoms and the brown algae) and the haptophytes (see selective pressures that drove this gene exodus and the Fig. 3). The chloroplast of the euglenophytes evolved mechanism by which it occurred are poorly understood, from a green alga, whereas the chloroplast of the other but the implications for the evolving chloroplast were groups (with the exception of certain dinoflagellates – profound. First, it had lost control of its own destiny see below) is probably derived from a red alga. In all of since it now possessed only a fraction of the genes needed for chloroplast biogenesis. The nucleus now controlled the growth and division of the organelle. Second, the expression of those genes that had remained in the chloroplast (mainly genes for components of the photosynthetic apparatus and the organelle’s trans- cription/translation apparatus) needed to be tightly co-ordinated with the expression of the nuclear genes that encoded chloroplast components. The nucleus therefore developed elaborate control mechanisms in which nuclear-encoded factors were targeted into the chloroplast to regulate chloroplast gene expression. Finally, the photosynthetic eukaryote had to solve a major logistical problem. The products of the nuclear- encoded genes were now being synthesized outside the chloroplast in the cytosol, whereas previously they had been made inside the organelle. An early modification to the fledgling chloroplast was therefore the development of a protein import system able to recognize the necessary proteins and transport them across the two membranes. From master to slave The eukaryotic algae that evolved from the original endosymbiosis had an advantage over their non- photosynthetic kin. They didn’t need to go hunting MICROBIOLOGY TODAY VOL 29/AUG 02 127 Further reading these groups, the old nucleus and all of the cytosolic has attracted considerable interest as a possible target for components have been lost completely. However, in