Complete Sequence of the Mitochondrial DNA of the Red Alga Porphyra purpurea: Cyanobacterial Introns and Shared Ancestry of Red and Green Algae

Abstract

The mitochondrial DNA (mtDNA) of Porphyra purpurea , a circular-mapping genome of 36,753 bp, has been completely sequenced. A total of 57 densely packed genes has been identified, including the basic set typically found in animals and fungi, as well as seven genes characteristic of protist and plant mtDNAs and specifying ribosomal proteins and subunits of succinate:ubiquinone oxidoreductase. The mitochondrial large subunit rRNA gene contains two group II introns that are extraordinarily similar to those found in the cyanobacterium Calothrix sp, suggesting a recent lateral intron transfer between a bacterial and a mitochondrial genome. Notable features of P. purpurea mtDNA include the presence of two 291-bp inverted repeats that likely mediate homologous recombination, resulting in genome rearrangement, and of numerous sequence polymorphisms in the coding and intergenic regions. Comparative analysis of red algal mitochondrial genomes from five different, evolutionarily distant orders reveals that rhodophyte mtDNAs are unusually uniform in size and gene order. Finally, phylogenetic analyses provide strong evidence that red algae share a common ancestry with green algae and plants. INTRODUCTIONHistorically considered to be "red plants," red algae (rhodophytes) were grouped together with protists only in the middle of this century; however, debate continues as to when this taxonomic group first appeared in the evolutionary history of mitochondria-containing eukaryotes. Because the red algal cell lacks flagellar basal bodies and centrioles, some workers have claimed that rhodophytes are the most early diverging and primitive group among photosynthetic eukaryotes (e.g., Lee, 1989). This view also has been suggested by certain molecular phylogenies (e.g., Lipscomb, 1989;Stiller and Hall, 1997). Some authors even advocate that red algae, in particular Cyanidioschyzon spp and Cyanidium spp, represent the evolutionary bridge between cyanobacteria and eukaryotes (Seckbach, 1994). An opposite interpretation contends that the red algae represent a derived group that has secondarily lost many of the distinctive features of the protistan cytoskeleton (Pueschel, 1990;Scott and Broadwater, 1990). Finally, it has been proposed that red algae may have given rise to the fungi (Demoulin, 1985) or that red algae are affiliated with the plant kingdom via common ancestry with green algae (see, e.g., Bhattacharya et al., 1993; Cavalier-Smith, 1993;McFadden et al., 1994;Schlegel, 1994;Paquin et al., 1997;Lang et al., 1998). This broad spectrum of coexisting, mutually exclusive hypotheses highlights our limited knowledge about the phylogenetic relationship between rhodophytes and other eukaryotic phyla.Rhodophytes form a morphologically heterogeneous phylum that has more species ( ‫ف‬ 2500 to 6000 in at least 12 orders; Woelkerling, 1990) than all other seaweeds combined. Multicellular as well as unicellular rhodophyte genera exist, and there is also considerable variety in morphology and physiology throughout the phylum. On the basis...

The Rhodomonas salina mitochondrial genome: bacteria-like operons, compact gene arrangement and complex repeat region

“…Third, genes encoding certain subunits of NADH dehydrogenase subunits and ATPase ( nad8 , nad10 , nad11 and atp1 ) are rarely found in eukaryotes. Fourth, subunits of succinate:ubiquinone oxidoreductase ( shd3 and sdh4 ) are present in only a few green algae and the liverwort Marchantia polymorpha (28–31), in several red algae (5,32–34) and in all jakobid flagellates including Reclinomonas americana (3,35). …”

“…Both tandem repeats and stem–loop structures described above might play a role in transcription and/or replication, as suggested for vertebrate animal mtDNAs (46–50). Similarly, in the mtDNA of the red alga Chondrus crispus , transcription has been shown to initiate at a bidirectional promoter that is close to a palindromic repeat (51), a feature also present in the red alga Porphyra purpurea (5). …”

“…the proportion of coding versus non-coding DNA. Highly compact mitochondrial genomes occur in animals [‘small is beautiful’ (4)], red algae (5), ciliates (6,7) and some fungi [e.g. Schizosaccharomyces pombe (8)], with the highest density found in the bicosoecid flagellate Cafeteria roenbergensis (9) where only 3.4% is non-coding.…”

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“…Second, in a number of cases, mitochondrial protein-coding clusters retain the gene order of their bacterial homologs, but these clusters exhibit mitochondrion-specific deletions that are most parsimoniously explained as having occurred in a common ancestor of mitochondrial genomes, subsequent to its divergence from the bacterial ancestor. Third, mitochondria form a monophyletic assemblage to the exclusion of bacterial species in phylogenetic reconstructions using concatenated protein sequences [8,9,25,27,28] as well in small-subunit rRNA trees [12]. …”

Identification of a new marine algal species Pyropia nitida sp. nov. (Bangiales: Rhodophyta) from Monterey, California

“…Examination of these two species in the field where they co-occur in Pacific Grove, found that the margins of freshly collected P. lanceolata are more strongly ruffled than P. nitida. The mitogenome of P. nitida is intermediate in length 35 313 bp (29 156 bp -Wildemania schizophylla to 42 268 bp -Pyropia tenera) and consistent in gene number with 53 genes (49 genes -P. perforata to 57 genes -P. yezoensis) to other published mitochondrial genomes for the family (Burger et al, 1999;Hwang et al, 2013;Kong et al, 2013;Mao et al, 2012;Reith & Munholland, 1995;Smith et al, 2012;Wang et al, 2013). Like P. nitida, five species in the Bangiaceae contain orf550, and four species orf831.…”