Algal Chloroplasts Secondary article Saul Purton, University College London, London, UK Article Contents . Introduction A great diversity of chloroplasts is found amongst the various algal groups. This diversity . Diversity and Classification of Algae is the result of an intriguing evolutionary process that involved the acquisition of . Origins and Evolution of Algal Chloroplasts chloroplasts by different eukaryotic organisms. Chloroplast Genetics and Molecular Biology . Protein Transport in the Chloroplast . Summary Introduction The chloroplast is one of a family of related biosynthetic and which lack the differentiated structures that organelles (termed plastids) found within the cells of define higher plants (roots, shoots, leaves, etc.). Indeed, plants, eukaryotic algae and certain protists. The primary the algae are often referred to as ‘lower’ or ‘primitive’ role of the chloroplast is the fixation of atmospheric carbon plants. Included within the algae are the prokaryotic through photosynthesis, but it is also the site of synthesis of cyanobacteria (formerly referred to as blue-green algae), many other important compounds including pigments, together with a diverse collection of microscopic and fatty acids, amino acids and nucleotides. Chloroplasts are macroscopic eukaryotes. Algal species can be unicellular, distinguishable from other plastid types in that they filamentous or multicellular and they range in size from the contain chlorophyll and other pigments that are involved unicellular forms that are only a few micrometres in in light energy capture and dissipation. In higher plants, diameter to the giant Laminaria seaweeds that are tens of nonphotosynthetic plastids such as chromoplasts, amylo- metres long. Algae have adapted to life in a wide range of plasts and leucoplasts are found in nongreen tissue and environments. Aquatic algae are found in all water bodies fulfil various biosynthetic and storage functions. Within – freshwater, seawater and brackish – whereas terrestrial the algae, this level of plastid differentiation is not seen and algae are found in soils, rocks and snow throughout the one plastid type prevails. Typically, algae possess chlor- world. oplasts, although those heterotrophic algae that have lost The principal feature that separates the eukaryotic photosynthetic function may retain a nonpigmented algae from other members of the kingdom Protista is plastid. This is certainly the case for the apicomplexans, a the presence of a chloroplast (although some algae group of parasitic protists that possess a plastid of possess nonphotosynthetic plastids and others have lost unknown function. their plastid completely). All algal chloroplasts possess The idea that chloroplasts evolved from photosynthetic chlorophyll a as their primary photosynthetic pigment. prokaryotes was first proposed by Mereschowsky nearly However, the nature of the accessory pigments varies one hundred years ago. Today, it is generally agreed markedly between the different algal groups. This that the original progenitor of all plastids was a cyano- difference in pigmentation has long been used in the bacterium that was engulfed by a nonphotosynthetic classification of algae, and allowed early phycologists to eukaryote cell some 1–2 billion years ago, and was retained define species as belonging to the ‘green algae’, ‘red algae’, within the cell as an endosymbiont. The modern-day ‘brown algae’, etc. The system of classification was descendants of this eukaryote–prokaryote chimaera in- subsequently refined using ultrastructural characteristics clude all plants, together with the green and red algae. of the cell, with particular emphasis on the chloroplast. Other algal groups almost certainly acquired their The number of membranes surrounding the chloroplast, chloroplasts ‘second-hand’ by engulfing other eukaryotic the presence and arrangement of chloroplast structures algae. It is this spread of the chloroplast during evolution such as the eyespot and the pyrenoid body, and the that has resulted in the many different algal groups found type of carbohydrate reserve within the cell, all serve as today. Consequently, chloroplast characteristics play a diagnostic aids to classification. This has led to a central role in the identification and classification of this classification system composed of ten major phyla as diverse group of organisms. outlined in Table 1. In the last twenty years, extensive DNA sequencing and the development of computational methods for Diversity and Classification of Algae comparing gene sequences, protein sequences or genome organization have led to a new discipline: molecular The term ‘alga’ encompasses a large and rather hetero- phylogenetics. This has proved to be a powerful tool in geneous collection of (mainly) photosynthetic organisms understanding the evolutionary relationships between the that are most commonly found in aquatic environments, algae. ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 1 2 Algal Chloroplasts ENCYCLOPEDIA OF LIFE SCIENCES / Table 1 The classification of the algae Phylum (= Division) Pigment contenta Number of chloroplast membranes Storage product Association of thylakoids Kingdom Prokaryota Cyanophyta 1. Cyanobacteria a, PB Free-living prokaryotes with Myxophycean starch Concentric, unstacked cell membrane bounded by 2. Oxychlorobacteria a, b, (c) peptidoglycan (PG) cell wall Starch-like compound Stack of 2–5 & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Kingdom Protista Glaucophyta a, PB 2, separated by PG wall Starch Concentric, unstacked Rhodophyta a, PB 2 Floridean starch Single, unstacked Chlorophyta a, b 2 Starch Stacks of 2–6 Cryptophyta a, c, PBb 4, nucleomorph Starch Paired stacks Chlorarachniophyta a, b 4, nucleomorph Paramylon Stacks of 1–3 Chromophyta (= Heterokontophyta) a, c 4 Chrysolaminaran Stacks of 3 Haptophyta (= Prymnesiophyta) a, c 4 Chrysolaminaran Stacks of 3 Euglenophyta a, b 3 Paramylon Stacks of 3 Dinophyta a, c 3 Starch Stacks of 3 aMajor pigments are chlorophylls a, b and c and phycobilins (PB). bPhycobilins are not contained within a phycobilisome. Algal Chloroplasts Origins and Evolution of Algal motility and scavenging of nutrients) were rapidly lost. Additional genes were eliminated by a process of gene Chloroplasts substitution in which host nuclear genes for key enzyme activities functionally replaced homologous bacterial Endosymbiosis – alandmarkinevolution genes. This probably involved the duplication of a nuclear Symbiosis and the establishment of the chloroplast gene and the redirecting of one of the gene products into the organelle almost certainly began when a unicellular fledgling organelle, resulting ultimately in the loss of the phagotrophic eukaryote engulfed an ancestral cyanobac- corresponding bacterial gene. Finally, and perhaps most terium. Instead of being digested as food, the cyanobacter- remarkably, there was a mass transfer of most of the ium was retained in the cell as an endosymbiont (Figure 1). remaining bacterial genes from the endosymbiont to the The eukaryote benefited from the carbohydrate generated nucleus. This gene transfer almost certainly involved a by the photosynthetic activity of the bacterium, and the three-step process that started with the escape of genetic bacterium found itself in a nutrient-rich and protected material (DNA or messenger RNA) from the endosym- niche. The growth and division of the bacterium allowed it biont compartment into the nucleus such that gene copies to be inherited as a component of the eukaryotic cell. were now present in both genomes. This was then followed However, the autonomy of the bacterium was soon lost as by the establishment of the nuclear copy as a functionally selective pressures resulted in a dramatic reduction in the expressed gene able to target its product back to the size and complexity of its genome. Of the several thousand endosymbiont. The original, and now redundant, gene was bacterial genes, those no longer required for an intracel- then lost from the endosymbiont genome. lular existence (e.g. genes required for cell wall synthesis, The nature of the driving force behind these gene substitution and gene transfer events is not known for certain, but is best explained by the genetics principle termed ‘Mu¨ ller’s ratchet’. This proposes that deleterious Phagotrophic eukaryote mutations accumulate more rapidly in asexually propa- gated genes (e.g. chloroplast genes) than in sexually Cyanophyte propagated ones (nuclear genes), since asexuality does Nucleus not allow the combining of different alleles and the subsequent elimination of mutations through recombina- Primary endosymbiosis tion and selection. Mu¨ ller’s ratchet is further exacerbated in the chloroplast since the photosynthetic process generates reactive oxygen species that can damage DNA. Green algae Selective pressures therefore ensured that a cyanobacter- Red algae ium that was once free-living and genetically autonomous Glaucophytes lost most of its genes and became an enslaved organelle dependent on the host nucleus for the majority of the genetic information required for its biogenesis. Secondary endosymbiosis Nucleomorph Cryptomonads Three extant lineages possess primary plastids Chlorarachniophytes As depicted in Figure 1, three major algal lineages have arisen as a result of the endosymbiotic process. In each Loss of nucleomorph case, the chloroplast is surrounded by two membranes and is defined as a primary plastid. The outer membrane