Algae and Their Chloroplasts with Particular Reference to the Dinoflagellates

Paleontological Research, vol. 10, no. 4, pp. 299–309, December 31, 2006 6 by the Palaeontological Society of Japan Algae and their chloroplasts with particular reference to the dinoflagellates TAKEO HORIGUCHI Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan (email: [email protected]) Received April 29, 2006; Revised manuscript accepted September 21, 2006 Abstract. This account firstly outlines the relationships between algal diversity and chloroplast acquisition through endosymbiosis. Secondly, it briefly reviews chloroplast diversity in dinoflagellates. Particular em- phasis is placed on the evolutionary process in the small but interesting group of dinoflagellates that possess a diatom endosymbiont. Key words: chloroplast, diatom endosymbiont, dinoflagellate, secondary endosymbiosis, tertiary endosymbiosis Diversity of eukaryotic algae Plantae (e.g., land plants and green algae, red algae and glaucophytes), Chromalveolata (e.g., Chromista The eukaryotic algae are an assemblage of [Hetrokontophyta, Haptophyta, Cryptophyta, oomy- chloroplast-bearing photosynthetic organisms. They cetes, bicosoecids and labyrinthulids] and Alveolata are extremely diverse in terms of morphology, cytol- [dinoflagellates, apicomplexa and ciliates]), Rhizaria ogy and life cycle (e.g., Hoek et al., 1995). The eukary- (e.g., Cercozoa and Radiolaria) and Excavata (e.g., otic algae can be classified into nine divisions, the Euglenoza, jacobids and diplomonads) or five ‘‘super- Rhodophyta, Chlorophyta, Glaucophyta, Heterokon- groups’’ (Keeling, 2004), viz., Unikonts (including tophyta (including Phaeophyceae (brown algae), Ba- Opisthokonta and Amoebozoa), Plantae, Chromal- cillariophyceae (diatoms), Chrysophyceae, Raphido- veolates, Rhizaria and Excavates (also see Cavalier- phyceae, Xanthophyceae and other minor groups), Smith, 2003, and Nozaki, 2005, for higher taxonomic Haptophyta, Cryptophyta, Dinophyta, Euglenophyta systems of eukaryotes). Not all the groups described and Chlorarachniophyta. Recent molecular phyloge- above, however, enjoy full support from the molecular nies indicate that, although each group is monophy- data—the Excavata, for example, are recognized only letic, many of them are totally unrelated, with closer when the molecular and morphological data are com- relationships to nonphotosynthetic protists (e.g., Eu- bined (Simpson and Roger, 2004b). By positioning the glenophyta and Kinetoplastida; Dinophyta and Cilio- organisms termed ‘algae’ on this global phylogenetic phora; etc.) (e.g., Cavalier-Smith, 1993a). The pres- tree of the eukaryotes, it readily become apparent ence of chloroplasts in these unrelated groups is due how diverse the algae are (for example, see Keeling, to chloroplast acquisition through independent endo- 2004, Figure 1). symbioses. The phylogenetic affinities of eukaryotic organisms, Origin of the chloroplast as a whole, are becoming clearer by the advancement of molecular phylogenetic studies, although discrepan- The obvious common feature that is shared by eu- cies between phylogenies derived from different genes karyotic algae is the presence of chloroplasts. The are encountered and some uncertainty exists with re- mechanism and timing of chloroplast acquisition in gard to the order of deep branches. Recent schemes each group are the key issues for understanding of for the classification of the eukaroyotes recognize six the origins of algae. It is widely accepted that the ‘‘kingdoms’’ (Simpson and Roger, 2004a), viz., Opis- chloroplast was acquired originally through endosym- thokonta (e.g., animals, choanoflagellates and fungi), biosis, i.e., a primitive heterotrophic eukaryote en- Amoebozoa (e.g., slime molds and lobose amoebae), gulfed a cyanobacterium-like photosynthetic prokar- 300 Takeo Horiguchi Figure 1. A hypothetical evolutionary sequence of acquisition of secondary chloroplast (Chromista-type) through secondary endosymbiosis (based on Cavalier-Smith, 1993b). A photosynthetic alga with primary plastid is engulfed by a heterotrophic eukaryote and retained in a food vacuole of the latter organisms (A and B). The food vacuole (phagosomal membrane) is fused with the outer nuclear envelope and the organelles of the engulfed alga disappear (C) (at this stage, the vestigial nucleus (nucleomorph) is retained). Finally, the secondary chloroplast surrounded by four membranes is established (D). HN: host nucleus, EN: endosymbiont nucleus. yote and eventually converted the endosymbiont into Origins of other algal chloroplasts a photosynthetic organelle (see Tomitani in this vol- ume and references therein). This process, resulting It is also widely accepted that chloroplasts in algae in the establishment of the first plant (alga), probably other than the three groups described above were took place only once in the history of life (see Archi- established by secondary endosymbioses (Archibald bald and Keeling, 2004; Keeling, 2004). This process is and Keeling, 2004; Keeling, 2004). In secondary endo- called chloroplast acquisition via ‘‘primary endosym- symbiosis, a phototrophic eukaryotic alga (with pri- biosis’’ and chloroplasts derived thus are called ‘‘primary chloroplasts) was engulfed by a heterotrophic mary chloroplasts.’’ The molecular data suggest that eukaryotic host and retained as an endosymbiont. only three extant photosynthetic groups are direct de- Subsequently, the organelles of the endosymbiont scendents of this first plant. These include the Chloro- (excepting the chloroplasts) were eventually lost phyta (including land plants), the Rhodophyta and the (Cavalier-Smith, 1993b) (Figure 1). In the case of sec- Glaucophyta. Because these three groups are very dif- ondary endosymbioses, the resulting chloroplasts, i.e., ferent in terms of morphology, photosynthetic pig- secondary chloroplasts, are enclosed by either three ment composition and mode of life cycles, e.g., the (Euglenophyta and Dinophyta) or four membranes red algae (Rhodophyta) are totally devoid of flagel- (Heterokontophyta, Haptophyta, Cryptophyta and lated stages, it is hard to believe that these three Chlorarachiniophyta), while in primary chloroplasts groups originate from a single ancestor. Such a mono- (Chlorophyta, Rhodophyta and Glaucophyta) they are phyletic relationship is supported by molecular work bounded by only two membranes. Two algal groups (Rodoriguez-Ezpeleta et al., 2005), although Nozaki with green chloroplasts, the Euglenophyta and the (2005) proposed that these three groups were para- Chlorarachniophyta, are thought to have acquired phyletic, situating them in a basal position of his king- their chloroplasts from green algae, while some other dom ‘‘Plantae.’’ groups, the Heterokontophyta, Haptophyta, Crypto- Dinoflagellates and their chloroplasts 301 phyta, and Dinophyta, are thought to have obtained the rest exhibit heterotrophic nutrition. Additionally, their chloroplasts from red algae. How many times plastid losses have been suggested to have occurred secondary endosymbioses have taken place for green independently multiple times in dinoflagellates (Sal- and red lineages, respectively, is still under discussion darriaga et al., 2001). (e.g., Cavalier-Smith, 2003, Bachvaroff et al., 2005). The types of chloroplasts found in dinoflagellates Members of the Cryptophyta and the Chlorarach- are classified into five categories: 1) a typical dinofla- niophyta are interesting as they retain, in addition to gellate ‘‘peridinin-type’’ chloroplast, 2) chloroplasts chloroplasts, a reduced nucleus (nucleomorph) of the of green algal origin (Figure 2), 3) chloroplasts of hap- endosymbiont, exhibiting an intermediate evolution- tophyte origin (Figure 3), 4) chloroplasts of diatom or- ary stage. The genomes of these two groups are well igin (Figure 4), and 5) kleptochloroplasts (Figure 5) studied (Douglas et al., 2001; Gilson and McFadden, and foreign algal components, whose level of perma- 2002). Although not usually regarded as algae, nency in incorporation into the host dinoflagellate members of the Apicomplexa, a group of parasitic (i.e., organelle versus food) is still uncertain. organisms including malarian parasites, are known to possess reduced chloroplasts, called apicoplasts (McFadden et al., 1996; Marećhal and Cesbron- Delauw, 2001). The apicoplast is also regarded as hav- ing been obtained via secondary endosymbiosis (Fast et al., 2001). Recently, a number of reviews dealing with the origins of secondary chloroplasts, the number of secondary endosymbioses and the validity of the ‘‘Chromal- veolata hypothesis’’ (Cavaler-Smith, 2004) have been published (for details, see Stobe and Maier (2002), Palmer (2003), Archibald and Keeling (2004), Keeling (2004), Bachwaroff et al. (2005), Harper et al. (2005), Nozaki (2005) and Yoon et al. (2005)). For the successful acquisition of secondary chloroplasts, a protein targeting system must be established and this topic is reviewed by Ishida (2005). Of all photosynthetic eukaryotes, the dinoflagellates are probably the most interesting with respect to chloroplast evolution because of their great diversity of chloroplast type. They therefore are briefly reviewed here. Chloroplast diversity in dinoflagellates The dinoflagellates are important members of aquatic ecosystems and some of them are known to produce red tides (Taylor and Pollingher, 1987). The dinoflagellates also produce cysts that preserve well and which have thus been well studied from a paleontological point of view (Fensome et al., 1993). Different

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