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Home , Eukaryote, Geosiphon, Glaucophyte, Nucleomorph

Going green: the of photosynthetic Saul Purton

The Look around our macroscopic world and evolutionary . Ultimately, the once autonomous is the site of you see a rich diversity of photosynthetic cyanobacterium became an integral and essential eukaryotes. A fantastic range of covers component of the eukaryotic – the chloroplast (see in and algal our land and numerous different macroalgae () Figs 1 and 2). This first truly photosynthetic 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 share a common legacy – the (green and all plants), the rhodophytes () important -containing (=chloroplast) that is and the . 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 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 and b, whereas the red than digested as food and a was established algae and glaucophytes have chlorophyll a only, together in which the host cell provided a protected and nutrient- with . Interestingly, the glaucophytes rich niche in return for the photosynthetic products have also retained the of the bacterium and generated by the bacterium. The story of how this their chloroplasts are bounded by an inner membrane bacterial evolved into a chloroplast and derived from the bacterial cell, a cell wall of peptido- was then spread by subsequent symbiotic events to and an outer membrane derived from the food other eukaryotes is a fascinating and on-going one 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 were the primary digestion, it was to pay a high price for its survival as a producers, utilizing the sun’s to convert carbon component of the eukaryotic cell. The several thousand dioxide to complex , and single-cell 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 Secondary symbiosis Primary symbiosis eukaryotes. The (also called blue-) 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 from water. These Green algae early cyanobacteria probably contained several different Red algae light-absorbing pigments, including 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 perhaps an attractive alternative to a quick meal, and Cryptophytes occasionally the death sentence would be commuted to imprisonment. Under this arrangement, the RIGHT: bacterium would be allowed to grow and divide within Fig. 1. The endosymbiotic its prison cell, and would therefore be retained and origin of chloroplasts. Note that the chloroplasts of euglenophytes and inherited by the eukaryote as it itself divided. Indeed, dinoflagellates actually have three examples of such endosymbiotic associations are 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 survives inside the cells of of the prey alga is the filamentous 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 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 (Glaucocystis), (b) discarded. Consequently, the algal cell was reduced to the red alga Porphyridium, (c) , 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 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 that intracellular existence (for example, those required for genes for the of the chloroplast were once obtained its chloroplast ) 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 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 to the eukaryotic nucleus. The and the ) 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/ 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 . 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 , whereas previously they had been made inside the organelle. An early modification to the fledgling chloroplast was therefore the development of a import system able to recognize the necessary 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 therapeutics, since the parasites’ hosts certainly Delwiche, C.F. (1999). Tracing the thread of plastid two other algal groups (the chlorarachniophytes and do not have . diversity through the tapestry the cryptophytes) a vestigial nucleus called the nucleo- of life. Am Nat 154, morph remains in the intermembrane , together A green ancestry for all? S164–S177. with a genetic system that allows and One of the most contentious suggestions to have Moreira, D. & Philippe, H. translation of the few hundred nucleomorph genes. emerged recently is that the primary endosymbiotic (2001). Sure facts and open Recent molecular analysis of the nucleomorph genome event occurred much earlier in eukaryotic evolution questions about the origin and has revealed that it has undergone a remarkable process than currently envisaged, and that many of today’s evolution of photosynthetic of compaction and miniaturization. The nucleomorph eukaryotic microbes have evolved from this plastids. Res Microbiol 152, genes are crammed together on three tiny chromo- photosynthetic ancestor. Limited support for this 771–780. somes, with non-coding DNA, such as and has come from phylogenetic studies of various , Purton, S. (2000). Algal intergenic DNA, reduced to an absolute minimum. and amoeboflagellates, which reveal the chloroplasts. In Encyclopedia The formation of the nucleomorph genome in the presence of cyanobacterial-like genes in their nuclear of Life Sciences, a web-based chlorarachniophytes and cryptophytes represents an . Just how far back we can trace the encyclopedia at www.els.net impressive case of convergent evolution since the photosynthetic ancestor must await further research, two groups have clearly evolved from independent but it is clear that the chloroplast was a ‘must have’ secondary endosymbiotic events. The chlorarachnio- accessory for many up-and-coming eukaryotes! phytes have green chloroplasts derived from a chloro- phyte, whereas the cryptophytes obtained their Saul Purton is a Reader in Molecular chloroplast from a red alga. Thus chloroplast in the Department of , University College acquisition by secondary endosymbiosis appears to London, Gower Street, London WC1E 6BT, UK. have occurred on at least six separate occasions, allowing Tel. 020 7679 2675; Fax 020 7679 7096 the emergence of a wide variety of photosynthetic email [email protected] eukaryotes. However, it didn’t stop there…

A change of colour The dinoflagellates represent perhaps the most fascinating and complicated of all the algal groups. The majority of photosynthetic dinoflagellates probably obtained their chloroplast by secondary endosymbiosis of a red alga. These chloroplasts are distinctive in that they contain the xanthophyll pigment peridinin, which gives a golden coloration to the chloroplast. However, approximately half of all dinoflagellate have no chloroplast at all and live life as phagotrophs. Others have green chloroplasts that appear to be of green algal descent, and others even have yellow-brown chloroplasts of origin (a case of tertiary endosymbiosis!). Recent phylogenetic analysis suggests that all dinoflagellates have evolved from a common ancestor that had a peridinin-containing chloroplast. It would appear therefore that the chloroplast has been subsequently lost by some dinoflagellates that reverted to a phagotrophic existence. Others have discarded their original chloroplast in favour of a new one from green algae or haptophytes. A further revelation has come from studies of the apicomplexan . These are obligate intracellular parasites and include the causative agents of malaria, toxoplasmosis and many other animal diseases. Remarkably, these organisms also seem to have a photosynthetic ancestry since they possess a non- pigmented plastid with its own tiny circular genome that is clearly a relic of a chloroplast genome, as described in Paul McKean’s article on pp. 129–131. This plastid

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