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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. [PUBLICATION ABSTRACT]

Pyramimonas vacuolata Suda, Horiguchi & Sym sp. nov. is described from Okinawa-jima Island, Japan. The species has been characterized using light and electron microscopy and its phylogenetic position inferred based on 18S rDNA and rbcL gene sequences relative to other species. Strains of P. vacuolata were isolated from coastal sand samples collected from two localities in Okinawa-jima. The cells are quadriflagellate but remarkably large for the genus, and the posterior half of the cell is vacuolated. The single parietal chloroplast is olive-green and contains two conspicuous pyrenoids lying on the same transverse plane, slightly anterior to the equatorial region of the cell. The pyrenoids are surrounded by numerous starch grains, and thylakoids randomly traverse the pyrenoid matrix. Two monolayered eyespots are present, situated on the same transverse plane as the pyrenoids. The alga possesses three types of body scales and four types of flagellar scales, inclusive of two types of hair scales. This species is readily distinguished from known species of Pyramimonas by its large cell size, the conspicuous posterior vacuole and the presence of two pyrenoids. The most obvious character of this species is its large posterior vacuole, and this prompted the adoption of the specific epithet 'vacuolata'. Analysis of 18S rDNA and rbcL gene sequences of P. vacuolata relative to those of other species of Pyramimonas shows that it falls, with strong support, in a monophyletic clade representing the subgenus Pyramimonas.

A new prasinophycean flagellate, Crustomastix didyma Nakayama, Kawachi & Inouye gen. & sp. nov., is described from the northwestern Pacific. This alga is elongate and bean-shaped and has two ventrally inserted, subequal flagella, with three types of hair scales. The entire cell and flagella are covered by a thin coat, which is probably derived from the Golgi apparatus and released through the duct system. The yellowish chloroplast is divided into two lobes connected by a narrow bridge. There is no pyrenoid or eyespot. The flagellar apparatus comprises the distal and proximal fibres, the Id and Is microtubular roots, and a duct fibre. A multilayered structure (MLS) is associated with the Id root. Some features, such as the swimming behaviour, the transitional region, and the absence of microtubular roots associated with the number 2 basal body, suggest a close relationship to the Mamiellales, but this alga differs from other members of the Mamiellales in having a MLS and a duct system, which are found in the Pyramimonadales. Crustomastix didyma appears to be the most primitive member of the Mamiellales found so far and retains some characters of a putative common ancestor of the Mamiellales and Pyramimonadales. The discovery of this unique prasinophycean alga provides new insights into the phylogeny and evolution of the green algae.