Article

The Chloroplast Genomes of the Green Algae Pyramimonas, Monomastix, and Pycnococcus Shed New light on the Evolutionary History of Prasinophytes and the Origin of the Secondary Chloroplasts of Euglenids

Département de Biochimie et de Microbiologie, Université Laval, Québec (Québec), Canada.
Molecular Biology and Evolution (Impact Factor: 9.11). 03/2009; 26(3):631-48. DOI: 10.1093/molbev/msn285
Source: PubMed

ABSTRACT

Because they represent the earliest divergences of the Chlorophyta and include the smallest known eukaryotes (e.g., the coccoid Ostreococcus), the morphologically diverse unicellular green algae making up the Prasinophyceae are central to our understanding of the evolutionary patterns that accompanied the radiation of chlorophytes and the reduction of cell size in some lineages. Seven prasinophyte lineages, four of which exhibit a coccoid cell organization (no flagella nor scales), were uncovered from analysis of nuclear-encoded 18S rDNA data; however, their order of divergence remains unknown. In this study, the chloroplast genome sequences of the scaly quadriflagellate Pyramimonas parkeae (clade I), the coccoid Pycnococcus provasolii (clade V), and the scaly uniflagellate Monomastix (unknown affiliation) were determined, annotated, and compared with those previously reported for green algae/land plants, including two prasinophytes (Nephroselmis olivacea, clade III and Ostreococcus tauri, clade II). The chlorarachniophyte Bigelowiella natans and the euglenid Euglena gracilis, whose chloroplasts originate presumably from distinct green algal endosymbionts, were also included in our comparisons. The three newly sequenced prasinophyte genomes differ considerably from one another and from their homologs in overall structure, gene content, and gene order, with the 80,211-bp Pycnococcus and 114,528-bp Monomastix genomes (98 and 94 conserved genes, respectively) resembling the 71,666-bp Ostreococcus genome (88 genes) in featuring a significantly reduced gene content. The 101,605-bp Pyramimonas genome (110 genes) features two conserved genes (rpl22 and ycf65) and ancestral gene linkages previously unrecognized in chlorophytes as well as a DNA primase gene putatively acquired from a virus. The Pyramimonas and Euglena cpDNAs revealed uniquely shared derived gene clusters. Besides providing unequivocal evidence that the green algal ancestor of the euglenid chloroplasts belonged to the Pyramimonadales, phylogenetic analyses of concatenated chloroplast genes and proteins elucidated the position of Monomastix and showed that the Mamiellales, a clade comprising Ostreococcus and Monomastix, are sister to the Pyramimonadales + Euglena clade. Our results also revealed that major reduction in gene content and restructuring of the chloroplast genome occurred in conjunction with important changes in cell organization in at least two independent prasinophyte lineages, the Mamiellales and the Pycnococcaceae.

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Available from: Claude Lemieux, Sep 08, 2015
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    • "1A and supplementary tables S1 and S2, Supplementary Material online). Among the 71 inteins found in eukarya, all had been previously described (supplementary table S3, Supplementary Material online) (Wang and Liu 1997; Butler et al. 2006; Poulter et al. 2007; Turmel, et al. 2009; Swithers, et al. 2013; Novikova et al. 2014). Of bacterial and archaeal species, 24% and 47%, respectively , contain inteins, with many of these harboring more than one, whereas only 1.1% of eukarya contain inteins with only one per genome (fig. "
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    • "2). Similar gene losses during secondary endosymbioses were proposed for the plastids in euglenophytes (Turmel, Gagnon, et al. 2009; Hrdá et al. 2012), chlorarachniophytes (Rogers et al. 2007; Tanifuji et al. 2014), heterokont algae (Oudot-Le Secq et al. 2007; Cattolico et al. 2008), cryptophytes (Khan et al. 2007), haptophytes (Sá nchez Puerta et al. 2005), and photosynthetic lineages basal to apicomplexan parasites (Janouškovec et al. 2010). Unfortunately, our current knowledge is insufficient to clarify the precise driving force(s) for the gene losses commonly observed among these plastids. "

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    • "2). Similar gene losses during secondary endosymbioses were proposed for the plastids in euglenophytes (Turmel, Gagnon, et al. 2009; Hrdá et al. 2012), chlorarachniophytes (Rogers et al. 2007; Tanifuji et al. 2014), heterokont algae (Oudot-Le Secq et al. 2007; Cattolico et al. 2008), cryptophytes (Khan et al. 2007), haptophytes (Sá nchez Puerta et al. 2005), and photosynthetic lineages basal to apicomplexan parasites (Janouškovec et al. 2010). Unfortunately, our current knowledge is insufficient to clarify the precise driving force(s) for the gene losses commonly observed among these plastids. "
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