Do red and green make brown?: perspectives on plastid acquisitions within chromalveolates

Abstract

The chromalveolate "supergroup" is of key interest in contemporary phycology, as it contains the overwhelming majority of extant algal species, including several phyla of key importance to oceanic net primary productivity such as diatoms, kelps, and dinoflagellates. There is also intense current interest in the exploitation of these algae for industrial purposes, such as biodiesel production. However, the evolution of the constituent species, and in particular the origin and radiation of the chloroplast genomes, remains poorly understood. In this review, we discuss current theories of the origins of the extant red alga-derived chloroplast lineages in the chromalveolates and the potential ramifications of the recent discovery of large numbers of green algal genes in chromalveolate genomes. We consider that the best explanation for this is that chromalveolates historically possessed a cryptic green algal endosymbiont that was subsequently replaced by a red algal chloroplast. We consider how changing selective pressures acting on ancient chromalveolate lineages may have selectively favored the serial endosymbioses of green and red algae and whether a complex endosymbiotic history facilitated the rise of chromalveolates to their current position of ecological prominence.

Fig. 1.

The amazing diversity of algae. A representative display of extant, chloroplast-containing eukaryotes is shown. The images shown were obtained by photography, bright-field light microscopy, and scanning electron microscopy. Scale bars within each image are 5 μm; images lacking scale bars are macroscopic. (A to E) Eukaryotes containing primary archaeplastid chloroplasts, Cyanophora sp. (glaucophyte), Champia parvula (red alga), Haematococcus pluvialis (green alga), Acetabularia sp. (green alga), and Cosmos atrosanguineus (plant). (F to J) Red-derived chloroplasts, Cryptomonas sp. (cryptomonad), Emiliania huxleyi (haptophyte), Fragilaria sp. (diatom), Laminaria hyperborea (kelp), and Ceratium horridum (dinoflagellate). (K to O) Other chloroplast lineages, Paulinella chromatophora (rhizarian, primary nonarchaeplastid), Euglena mutabilis (euglenozoan, green secondary), Gymnochlora stellata (rhizarian, green secondary), Karenia mikimotoi (dinoflagellate, haptophyte tertiary), and Plasmodium falciparum (apicomplexan, nonphotosynthetic remnant chloroplast). Images A to D, F, G, and K to M are reprinted from the Encyclopedia of Life (http://www.eol.org); images H, J, and N are from the Culture Collection of Algae and Protozoa website (http://www.ccap.org); image O is from the Public Health Image Library, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services (http://phil.cdc.gov); and image E is used with permission from Philippe Giabbanelli. All images are used under the Creative Commons License.

Fig. 2.

Algae across the eukaryotes. Presented is a tree of eukaryotes, based on data from reference , showing the six “supergroups.” For ease of visualization, the SAR clade has been split into its three constituent lineages (stramenopiles, alveolates, and rhizaria). Chromalveolate groups are shaded in orange. Photosynthetic phyla are shown in colored text to indicate the chloroplast lineage, as shown in the key. The majority have just one lineage, but for some (dinoflagellates and cercozoa) there are two or more. Nonphotosynthetic phyla that contain organelles believed to be derived from ancestral chloroplasts are in italics.

Fig. 3.

Four hypotheses for the origin of green genes in diatoms. The schematic shows the potential endosymbiotic progressions from an ancient, nonphotosynthetic ancestor of the chromalveolates to extant diatoms which contain red-derived chloroplasts and a mosaic of red and green genes in the nucleus. Green genes are depicted as arising via four possible pathways: A, recent lateral gene transfer; B, ancient secondary endosymbiosis; C, recent secondary endosymbiosis; D, tertiary endosymbiosis of a haptophyte. For clarity, pathway D is subdivided into two sections, stramenopiles and haptophytes, with arrows depicting the divergent evolutionary history of each lineage.

Fig. 4.

Model of the evolution of chromalveolate chloroplasts. Based on the distribution of green and red algal genes in chromalveolate nuclear genomes, the model shown suggests that (i) chromalveolates are monophyletic, (ii) they acquired a secondary green alga-derived chloroplast prior to the divergence of the CCTH and SAR clades, (iii) this chloroplast was subsequently replaced via the concerted secondary endosymbiosis of a red alga by an ancient member of the CCTH clade and tertiary endosymbiotic transfers from the CCTH clade into the SAR clade, and (iv) these chloroplasts were themselves secondarily lost by the nonphotosynthetic members of the CCTH clade, the apicomplexa and perkinsids. For clarity, lineage-specific endosymbiotic events within the rhizaria, katablepharids, and dinoflagellates are omitted.

Fig. 5.

A history of algal evolution. The timeline maps changes in atmospheric composition and global extinction events from the end of the Precambrian to the present. Vertical arrows indicate the origins of key photosynthetic eukaryotic lineages as determined from fossil records (A, 1 to 4) or from fossil constrained molecular data (B to D). (A to D) Algae: A, archaeplastids; B, dinoflagellates; C, haptophytes; D, diatoms. (0 and 2 to 4) Plants: 0, early land plants (embryophytes); 2, vascular plants; 3, conifers; 4, flowering plants. This image was created from data provided by the ENSEMBLE project (2, 8, 57, 77, 106, 107) and H. Griffiths, University of Cambridge (personal communication).