The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA

Abstract

BackgroundDunaliella salina Teodoresco, a unicellular, halophilic green alga belonging to the Chlorophyceae, is among the most industrially important microalgae. This is because D. salina can produce massive amounts of β-carotene, which can be collected for commercial purposes, and because of its potential as a feedstock for biofuels production. Although the biochemistry and physiology of D. salina have been studied in great detail, virtually nothing is known about the genomes it carries, especially those within its mitochondrion and plastid. This study presents the complete mitochondrial and plastid genome sequences of D. salina and compares them with those of the model green algae Chlamydomonas reinhardtii and Volvox carteri.ResultsThe D. salina organelle genomes are large, circular-mapping molecules with ~60% noncoding DNA, placing them among the most inflated organelle DNAs sampled from the Chlorophyta. In fact, the D. salina plastid genome, at 269 kb, is the largest complete plastid DNA (ptDNA) sequence currently deposited in GenBank, and both the mitochondrial and plastid genomes have unprecedentedly high intron densities for organelle DNA: ~1.5 and ~0.4 introns per gene, respectively. Moreover, what appear to be the relics of genes, introns, and intronic open reading frames are found scattered throughout the intergenic ptDNA regions -- a trait without parallel in other characterized organelle genomes and one that gives insight into the mechanisms and modes of expansion of the D. salina ptDNA.ConclusionsThese findings confirm the notion that chlamydomonadalean algae have some of the most extreme organelle genomes of all eukaryotes. They also suggest that the events giving rise to the expanded ptDNA architecture of D. salina and other Chlamydomonadales may have occurred early in the evolution of this lineage. Although interesting from a genome evolution standpoint, the D. salina organelle DNA sequences will aid in the development of a viable plastid transformation system for this model alga, and they will complement the forthcoming D. salina nuclear genome sequence, placing D. salina in a group of a select few photosynthetic eukaryotes for which complete genome sequences from all three genetic compartments are available.

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

“…Mitochondrial and plastid genome size can vary by orders of magnitude, but mtDNAs exhibit a wider range of sizes, both among and within lineages, than ptDNAs (40,55). At one extreme are the giant mtDNAs of seed plants, like cucumber (∼1.6 Mb) (49) and Silene conica (∼11 Mb) (40), as well as those of diplonemids, which can exceed 500 kb (51).…”

“…Most of the variation in organelle genome size is due to differences in noncoding DNA content (26), which varies from ∼1% to 99% for mtDNAs (40) and from ∼5% to 80% for ptDNAs (55). Small organelle genomes, such as vertebrate mtDNAs and apicomplexan ptDNAs, are usually codingdense and devoid of introns, whereas large genomes, including the S. conica mtDNA and V. carteri ptDNA, are distended with noncoding nucleotides.…”

“…Small organelle genomes, such as vertebrate mtDNAs and apicomplexan ptDNAs, are usually codingdense and devoid of introns, whereas large genomes, including the S. conica mtDNA and V. carteri ptDNA, are distended with noncoding nucleotides. These noncoding regions are often riddled with repeats, introns, mobile elements, and, for mitochondrial genomes, foreign DNA (6,26,55). The number of introns within organelle genomes can differ from none (e.g., human mtDNA) to >150 (65), and mitochondria generally display more intronic variability than plastids (26), although euglenid plastids are a notable exception.…”

“…RNA splintering has gone even further in the P. falciparum mtDNA, where at least 27 distinct modules encode the LSU and SSU rRNAs (73). Fragmented ptDNA-located genes are uncommon (5) but have been documented in chlamydomonadalean algae (55), peridinin dinoflagellates (74), C. velia (47), and the haptophyte-derived plastid of the dinoflagellate Karlodinium veneficum (54). Also, rps12 is transspliced in the plastids of various land plants (13).…”

“…In Dunaliella salina and Volvox carteri, both the mitochondrial and plastid genomes have undergone massive expansions, resulting in uncharacteristically long intergenic regions and large amounts of repetitive DNA (Table S2) (27,55). What's more, similar repeats exist in the mtDNA and ptDNA of each alga (27,55).…”