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Cryptophytes are an ecologically important group of largely photosynthetic unicellular eukaryotes. This lineage is of great interest to evolutionary biologists because their plastids are of red algal secondary endosymbiotic origin and the host cell retains four different genomes (host nuclear, mitochondrial, plastid, and red algal nucleomorph). Here, we report a comparative analysis of plastid genomes from six representative cryptophyte genera. Four newly sequenced cryptophyte plastid genomes of Chroomonas mesostigmatica, Ch.
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Placoidea, Cryptomonas curvata, and Storeatula sp. CCMP1868 share a number of features including synteny and gene content with the previously sequenced genomes of Cryptomonas paramecium, Rhodomonas salina, Teleaulax amphioxeia, and Guillardia theta. Our analysis of these plastid genomes reveals examples of gene loss and intron insertion. In particular, the chlB /chlL/ chlN genes, which encode light-independent (dark active) protochlorophyllide oxidoreductase (LIPOR) proteins have undergone recent gene loss and pseudogenization in cryptophytes. Comparison of phylogenetic trees based on plastid and nuclear genome data sets show the introduction, via secondary endosymbiosis, of a red algal derived plastid in a lineage of chlorophyll- c containing algae. This event was followed by additional rounds of eukaryotic endosymbioses that spread the red lineage plastid to diverse groups such as haptophytes and stramenopiles. Introduction The cryptophyte algae (= cryptomonads) are an evolutionarily distinct and ecologically important unicellular eukaryotic lineage inhabiting marine, brackish water, and freshwater environments (; ).
Cryptophytes are mostly photosynthetic with plastids that contain chlorophyll- a and -c, as well as phycobilins as accessary pigments. They are comprised of brown-, red-, or blue-green-colored photosynthetic groups (;; ), colorless nonphotosynthetic groups including Cryptomonas paramecium with a secondarily reduced plastid genome (), and heterotrophic Goniomonas species that lack plastids (;;;; ). Cryptophyte plastids are bounded by two inner and two outer envelope membranes. The outermost membrane is continuous with the endoplasmic reticulum (i.e., chloroplast ER; CER), which is connected to the outer membrane of the nuclear envelope. The nucleomorph, the remnant nucleus derived from the red algal progenitor of the cryptophyte plastid, is located between the two pairs of inner and outer plastid membranes (;; ). Cryptophyte cells contain four genomes: host-derived nuclear and mitochondrial genomes, and plastid and nucleomorph genomes of red algal endosymbiotic origin. Given this unusual feature, cryptophytes provide direct evidence of secondary endosymbiotic events occurring between phagotrophic and photoautotrophic eukaryotes (; ), a process that presumably occurred in several other protist lineages (e.g., euglenoids, chlorarachniophytes;; ).
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