Evolutionary History: Four Genomes in a Cell

Cryptophytes resemble Russian dolls. Due to a successive series of endosymbiotic events, at least four different formerly separate organisms became nested within each other to combine to one lifeform (McFadden 2001; Reyes-Prieto et al. 2007; Fig. 1). Each of the organisms contributed its genome, thus four different genomes are present in a cryptophyte cell.

The Presumed Endosymbiotic Events in Chronological Order

evolution of the cryptophyte plastid

Thus, a photosynthetic cryptophyte cell contains two linear eukaryotic genomes (host cell nucleus with the majority of DNA and nucleomorph = former red algal nucleus) and two circular prokaryotic genomes (a former α-proteobacterial and a former cyanobacterial genome). Red algae produce starch as an energy storage in the cytoplasm, not in the plastid as in green algae or land plants. Thus, it can be deduced from the eukaryotic ribosomes and the starch grains between the two inner and the two outer plastid membranes, that the periplastidial space corresponds to the former cytoplasm of the engulfed red alga. Complete nucleomorph genomes have been sequenced from Guillardia theta and Hemiselmis andersenii (Douglas et al. 2001; Lane et al. 2007) and two complete plastid genomes are available (Guillardia theta and Rhodomonas salina; Douglas and Penny 1999; Khan et al. 2007). Also a complete mitochondrial genome of a Rhodomonas salina strain has been sequenced (Hauth et al. 2005).

Cryptophytes are not the only algae with complex plastids derived from a secondary endosymbiosis. Complex plastids with more than two surrounding membranes are also found in stramenopile algae (brown algae, diatoms, eustigmatophytes, golden algae, raphidophytes), in photosynthetic dinoflagellates, in haptophytes, in euglenoids or in chlorarachniophytes (Reyes-Prieto et al. 2007). Only in the chlorarachniophytes, amoebae with a complex plastid of green algal origin, also a nucleomorph is found – in this case the former nucleus of a green alga (Gilson et al. 2006).

evolution of the cryptophyte plastid

Evolution of the Unique Cryptophyte Biliproteins

The plastids of red algae and glaucophytes inherited their light harvesting complexes – the phycobilisomes – from the former cyanobacterial endosymbiont (MacColl 1998; Stirewalt et al. 1995; Ohta et al. 2003). Like the chlorophyll-containing light harvesting complexes they are attached to the outside of the plastid endomembrane system (the thylakoids). Phycobilisomes comprise several biliproteins (allophycocyanins, phycocyanins and in many red algae also phycoerythrins). Allophycocyanins and phycocyanins are blueish, phycoerythrins red. In cryptophytes, all genes for allophycocyanins and phycocyanins seem to have been lost and the remaining phycoerythrin has been transferred into the thylakoid lumina (Gantt et al. 1971; Apt et al. 1995; Fig. 2). Its subunit structure changed from (αβ)3 or (αβ)6 to (αβ)(α'β) (Glazer and Wedemayer 1995). The gene for the β-subunit is plastid-encoded, whereas the genes for the α-subunits, comprising at least two different genes, have been transferred to the nucleus (Gould et al. 2007). By exchange of the tetrapyrrole chromophores, the phycoerythrin changed colour and absorption spectrum in several cryptophyte lineages. As a result, not only different red, but also blue types of phycoerythrins (cryptophyte “phycocyanins”) evolved (Hill and Rowan 1989; Glazer and Wedemayer 1995). Despite of the profound changes in structure and of the the peculiar intra-thylakoidal organisation, the cryptophyte biliproteins seem to operate as active light-harvesting complexes (Doust et al. 2006).

Closest Relatives

The next related group to the cryptophytes apparently are the katablepharids, phagotrophic flagellates with explosive organelles resembling modified cryptophyte ejectosomes (Okamoto and Inouye 2005). Since the haptophytes grouped in previous phylogenetic analyses as a sister to cryptophytes and katablepharids, the three taxa have been united under the name Hacrobia (Patron et al. 2007; Okamoto et al. 2009). The chromalveolate hypothesis assumes that Hacrobia, Stramenopiles, ciliates, dinoflagellates and Apicomplexa are monophyletic and can be merged in one supergroup or kingdom Chromalveolata (Cavalier-Smith 1999). Whereas in phylogenetic trees inferred from supermatrices of plastid-encoded or nuclear-encoded plastid-targeted genes, support for the chromalveolate hypothesis is found, phylogenies inferred from genes of the host cell contradict this hypothesis (Yoon et al. 2002; Harper and Keeling 2003; Bachvaroff et al. 2005; Hackett et al. 2007; Yoon et al. 2008).