After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c

Abstract

The chromalveolate hypothesis proposed by Cavalier-Smith (J Euk Microbiol 46:347-366, 1999) suggested that all the algae with chlorophyll c (heterokonts, haptophytes, cryptophytes, and dinoflagellates), as well as the ciliates, apicomplexans, oomycetes, and other non-photosynthetic relatives, shared a common ancestor that acquired a chloroplast by secondary endosymbiosis of a red alga. Much of the evidence from plastid and nuclear genomes supports a red algal origin for plastids of the photosynthetic lineages, but the number of secondary endosymbioses and the number of plastid losses have not been resolved. The issue is complicated by the fact that nuclear genomes are mosaics of genes acquired over a very long time period, not only by vertical descent but also by endosymbiotic and horizontal gene transfer. Phylogenomic analysis of the available whole-genome data has suggested major alterations to our view of eukaryotic evolution, and given rise to alternative models. The next few years may see even more changes once a more representative collection of sequenced genomes becomes available.

Oxygenic photosynthesis and the distribution of chloroplasts

“…It is widely accepted that chloroplasts are derived from a single one-time event where a cyanobacterium was taken up into a eukaryotic single-celled organism (Delwiche 1999) which formed the base for all eukaryotic photosynthetic organisms (Green 2010;Ryes-Prieto et al 2008;Yoon et al 2004). This idea has become a paradigm that is widely illustrated in text books and continues to have considerable support from phylogenomic analyses (Hackett et al 2007;Keeling 2010).…”

“…In spite of numerous publications, the debate continues (cf. in Green 2010;Baurian et al 2010;Deschamps and Moreira 2009;Janouškovec et al 2010;Keeling 2010;Nozaki et al 2009;Ryes-Prieto et al 2008;Stiller 2007 was one chloroplast origin, and if so, what was the most likely host, i.e., is there only one Cinderella slipper and where is the best fit? Some unambiguous structural signs of symbiotic and/or endosymbiotic events were found some years ago when Gibbs (1981) provided significant examples showing that some chloroplasts had two limiting membranes (green and red algae), others were surrounded by three membranes (euglenids, dinoflagellates), while still others had four chloroplast membranes (browns, diatoms, cryptophytes) usually with an additional set of ribosomes on the ''chloroplast endoplasmic reticulum.''…”

“…Other groups, with Chl a and b pigmentation, are euglenids and chlorarachniophytes for which two separate secondary endosymbioses have been suggested (Green 2010, Fig. 1) but with distinctly different hosts.…”

“…The chromalveolates are a diverse grouping distinguished by: the presence of Chl a plus Chl c, carotenoid-type fucoxanthin or peridinin, having ciliated or flagellated hosts, and by some un-pigmented members having presumably lost a once functioning integrated chloroplast. Significant aspects of the chromalveolate hypothesis and major questions are provided by Green (2010) in a critical synopsis. She points out some of the unresolved problems, such as trying to reconcile the wide diversity of hosts with a single red algal endosymbiosis and the positioning of un-pigmented species.…”

“…At the organismal level, some of the biggest questions are: what were the original key characteristics from which the photosynthetic reaction centers were derived (Allen and Williams 2010), what essential changes were required for electron production by the water splitting complex (Williamson et al 2010), and what is the evidence for the timeline of how long cyanobacteria have been around (Schopf 2010)? Present day chloroplasts, presumably all derived originally from one cyanobacterial endosymbiotic event, have become dispersed in single-celled eukaryotic ''hosts'' with the greatest dispersion among the chlorophyll c-containing algae (Green 2010). Numerous examples of symbiotic stages of photosynthetic organisms in multicellular animals (Johnson 2010) lead to the interesting possibility that many of these are present day examples of chloroplast evolution in action, i.e., possible progressions from the symbiotic toward the endosymbiotic state.…”