The Origin, Losses and Gains of Chloroplasts

Abstract

Chloroplasts originated, probably once only, from a symbiotic cyanobacterium about 700–900 million years ago, and subsequently diversified in pigmentation, in patterns of thylakoid stacking, and in envelope structure, to produce all the major types of eukaryotic algae. Dinoflagellates and the two subkingdoms [Viridiplantae (green plants) and Biliphyta (red algae and glaucophytes)] of the kingdom Plantae probably diverged directly from a phagotrophic Cyanophoral Colponema-like biflagellate protozoan that already had a chloroplast. During the same epoch two independent lateral transfers of some of these early diverging chloroplasts (and of nuclear genes coding for some of their proteins) occurred by the endosymbiotic merger of two eukaryote cells. These secondary symbioses yielded one major predominantly photosynthetic taxon, the kingdom Chromista, and a minor algal class (Chlorarachnea) containing only the green reticulate amoeboflagellate genus Chlorarachnion. It has been suggested that the green chloroplasts of Euglena and the other members of the euglenoid class Euglenophyceae also arose by a secondary symbiosis involving a eukaryotic alga (possibly a green alga). However, more and more evidence supports the alternative view that no secondary symbiosis was involved, and that the euglenoid chloroplast is simply the earliest diverging of all and arose directly from the same cyanobacterium as all other chloroplasts. The prochlorobacteria (Prochloron, Prochlorothrix and Prochlorococcus) are cyanobacterial derivatives not specifically related either to green plant or to euglenoid chloroplasts, and are probably not even a monophyletic group: chlorophyll b probably evolved 4 times independently, thrice in photosynthetic bacteria and once in chloroplasts. Photosynthesis has been frequently lost by both bacteria and eukaryotes. However plastids have probably never been lost by plants, but have been lost (rarely: at least thrice) by chromists and (frequently: at least 30 times) by dinoflagellates. How often they have been lost by euglenoids is unclear. I propose that they were also lost, independently, by at least one protalveolate dinozoan flagellate, the ancestor of extant protalveolates (e.g. Colponema) and of Ciliophora and Apicomplexa, and by the ancestral opalozoan flagellate, from which most other non-photosynthetic protozoa including the choanoflagellate ancestors of animals and fungi probably evolved. I propose that chloroplasts originated in a tetrakont protozoan host, from which a biflagellate photo-phagotrophic lineage evolved that very soon gave rise to the euglenoids and other euglenozoa on the one hand and to the photo-phagotrophic common ancestor of the Dinozoa (dinoflagellates plus Protalveolata), the Plantae, and the Opalozoa on the other. I suggest that the symbiotic origin of chloroplasts directly stimulated the origin of Golgi dictyosomes, and of several other relatively advanced eukaryotic features including nuclear spliceosomal introns and the trans-splicing of 5’ mini-exons in Euglenozoa. The evidence and reasons for these conclusions are outlined.