J. Phycol. 39, 259–267 (2003) MINIREVIEW THE MESOZOIC RADIATION OF EUKARYOTIC ALGAE: THE PORTABLE PLASTID HYPOTHESIS1 Daniel Grzebyk,2 Oscar Schofield Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, 71 Dudley Road, New Brunswick, New Jersey 08901, USA Costantino Vetriani Department of Biochemistry and Microbiology, and Institute of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, 71 Dudley Road, New Brunswick, New Jersey 08901, USA and Paul G. Falkowski Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences and Department of Geology, Rutgers, The State University of New Jersey, 71 Dudley Road, New Brunswick, New Jersey 08901, USA Although all chloroplasts appear to have been de- In eukaryotic algae, all plastids are derived from a rived from a common ancestor, a major schism oc- common photoautotrophic prokaryotic ancestor and curred early in the evolution of eukaryotic algae that were sequentially appropriated by various nonphoto- gave rise to red and green photoautotrophic lin- synthetic host cells through primary, secondary, and eages. In Paleozoic and earlier times, the fossil even tertiary endosymbiotic events (Wolfe et al. 1994, record suggests that oceanic eukaryotic phytoplank- Delwiche 1999, Tomitani et al. 1999). Based on bio- ton were dominated by the green (chl b-containing) chemical and ultrastructural features of their plastids algal line. However, following the end-Permian ex- (van den Hoek et al. 1995), eukaryotic algae can be tinction, a diverse group of eukaryotic phytoplank- clustered into two major groups: a “green” and a “red” ton evolved from secondary symbiotic associations lineage. The green lineage comprises the Kingdom in the red (chl c-containing) line and subsequently Viridiplantae, which includes all green algae (Chloro- rose to ecological prominence. In the contemporary phyta) and higher plants (Streptophyta), all of which oceans, red eukaryotic phytoplankton taxa continue have primary endosymbionts. Two green algal phyla to dominate marine pelagic food webs, whereas the have secondary endosymbiotic plastids (euglenophytes green line is relegated to comparatively minor eco- and chlorarachniophytes), but both contain relatively logical and biogeochemical roles. To help elucidate few species. In the red lineage, the red algae per se why the oceans are not dominated by green taxa, we (Rhodophyta), which have plastids derived from a pri- analyzed and compared whole plastid genomes in mary endosymbiotic event, contain relatively few ex- both the red and green lineages. Our results suggest tant taxa and very few unicellular members. In con- that whereas all algal plastids retain a core set of trast to the green lineage, most eukaryotic algal taxa genes, red plastids retain a complementary set of that contain plastids from the red line are products of genes that potentially confer more capacity to auton- secondary or tertiary endosymbioses. These include omously express proteins regulating oxygenic photo- the dinoflagellates (Dinophyta) and the Kingdom synthetic and energy transduction pathways. We hy- Chromista comprised, in part, of haptophytes, crypto- pothesize that specific gene losses in the primary phytes, and heterokonts (including diatoms, brown endosymbiotic green plastid reduced its portability algae, and raphidophytes). for subsequent symbiotic associations. This corollary In Paleozoic and earlier eras, the fossil record of of the plastid “enslavement” hypothesis may have acritarchs is interpreted to contain taxa associated limited subsequent evolutionary advances in the with the extant prasinophyte green algae, suggesting green lineage while simultaneously providing a com- that members of the green lineage dominated eukary- petitive advantage to the red lineage. otic phytoplankton communities in the oceans (Tap- Key index words: endosymbiosis; evolution; phytoplank- pan 1980, Lipps 1993, Mendelson 1993). After the ton; plastid genome; RUBISCO end-Permian extinction, however, several unicellular algal phyla with secondary red plastids rose to ecologi- cal prominence. Although the possibility that second- ary symbiotic associations occurred in the red lineage 1Received 6 June 2002. Accepted 30 October 2002. before the end-Permian extinction cannot be ex- 2Author for correspondence: email [email protected]. cluded, the fossil evidence suggests that thecate di- 259 260 DANIEL GRZEBYK ET AL. noflagellates appeared in the early to mid-Triassic and core set of plastid genes intensively radiated in the Jurassic period (Bujak and At the time of this writing, we located 24 complete Williams 1979, Fensome et al. 1996), the coccolitho- chloroplast genome sequences in public databases; 10 phorids (Haptophyta) evolved in the late Triassic and are from algae (Table 1). We do not include in our rose to ecological prominence in the Cretaceous analysis the plastid genome of dinoflagellates, for (Roth 1987, Bown et al. 1992), and the diatoms which the current knowledge remains fragmentary at emerged sometime in the Jurassic and rose to ecologi- best (Boczar et al. 1991, Zhang et al. 1999, Barbrook cal prominence from the late Cretaceous (Lipps 1993, and Howe 2000). Gene distributions in the nine pho- Harwood and Nikolaev 1995). These phyla continue tosynthetic algal plastid genomes (excluding the non- to dominate the eukaryotic phytoplankton assem- photosynthetic Astasia longa) were established with the blages in the contemporary ocean. Although green 190 identified and 66 hypothetical (ycf ) protein-coding eukaryotic phytoplankton have not been competi- genes from the last update of plastid gene nomencla- tively excluded from the ocean (indeed, quantitative ture and distribution (Stoebe et al. 1998) (Table 2). molecular analyses suggest that prasinophytes remain The distribution reveals a set of approximately 50 relatively abundant in picoplankton; Moon-Van Der core protein-coding genes retained in all taxa (Fig. 1). Staay et al. 2001, Vaulot et al. 2002), green eukaryotic These genes are broadly clustered into three major phytoplankton seldom dominate in contemporary pe- functional domains: 1) genes encoding for the proton lagic marine ecosystems. For example, an analysis of coupled ATP synthase (atp genes); 2) genes encoding HPLC-based pigments composition from the Joint for photosynthetic processes, including reaction cen- Coastal Ocean Flux Study reveals that chl c is 3.4 times ter proteins (psa, psb genes), most of the electron more abundant in the ocean than chl b on a molar ba- transport components that connect the two photosys- sis (Falkowski, unpublished data). Why have red plas- tems (pet genes), and the large subunit of RUBISCO tid-containing phyla become so ecologically successful (rbcL genes); and 3) housekeeping genes that include over the past 250 million years? the plastid ribosomal proteins (rpl, rps genes), RNA Why plastids (or any other organelle) retain any polymerase (rpo genes), and elongation factor (tufA genetic information at all is unclear (Allen and Raven gene). Only one biosynthetic gene, involved in chl 1996). It is clear, however, that no plastid is com- synthesis (chlI ), is retained in all photosynthetic al- pletely autonomous, that is, capable of growth and gae; this gene was transferred to the nucleus in higher replication outside of the host cell. The reason is that plants. In the heterotrophic A. longa, the plastid ge- after all symbiotic events, most protoplastid genes nome retained mostly housekeeping genes, losing all were transferred to the host cell nucleus (McFadden but one (rbcLg) gene involved in photosynthesis. 1999). However, all plastids retain a set of genes that Among glaucophytes, the third primary endosymbi- are essential for the physiological function of the or- otic phylum with a few, rare, extant species, Cyano- ganelle in oxygenic photosynthesis. Here we present an phora paradoxa retains about 30 genes in common with analysis of whole plastid genomes from various eukary- all red plastids (rhodophytes, cryptophytes, and dia- otic algal taxa in an attempt to understand what ge- toms) and about 10 additional genes found only in netic features distinguish the two major plastid lineages rhodophytes but only 3 to 4 genes associated with from each other. From our analysis, we suggest that dif- green algal plastids (including the rbcLg gene coding ferences in gene composition between plastid geno- for the type IB large subunit of RUBISCO). types could account, in part, for the ecological success of phytoplankton containing secondary red plastids. In considering the relative ecological and evolu- tionary success of the red plastid phyla, we postulated Table 1. The algal plastid genomes available in databases. that genetic information retained by plastids is critical Number of in defining the potential fitness of the plastid in new protein-coding endosymbiotic associations. This hypothesis suggests Algal division, species, and reference genes that after a major selection event, such as a change in Rhodophyta (primary red plastids) redox chemistry of the ocean, red and green plastids Porphyra purpurea (Reith and Munholland 1995) 203 effectively compete with each other for accommoda- Cyanidium caldarium (Glöckner et al. 2000) 199 tion within new host cells. Assuming that, before the Cryptophyta (secondary red plastids) symbiotic association, the host cell did not contain Guillardia theta (Douglas