Abstract
Chlorarachniophyte algae possess four DNA-containing compartments per cell, the nucleus, mitochondrion, plastid and nucleomorph, the latter being a relic nucleus derived from a secondary endosymbiont. While the evolutionary dynamics of plastid and nucleomorph genomes have been investigated, a comparative investigation of mitochondrial genomes (mtDNAs) has not been carried out. We have sequenced the complete mtDNA of Lotharella oceanica and compared it to that of another chlorarachniophyte, Bigelowiella natans. The linear mtDNA of L. oceanica is 36.7 kbp in size and contains 35 protein genes, three rRNAs and 24 tRNAs. The codons GUG and UUG appear to be capable of acting as initiation codons in the chlorarachniophyte mtDNAs, in addition to AUG. Rpl16, rps4 and atp8 genes are missing in L.oceanica mtDNA, despite being present in B. natans mtDNA. We searched for, and found, mitochondrial rpl16 and rps4 genes with spliceosomal introns in the L. oceanica nuclear genome, indicating that mitochondrion-to-host-nucleus gene transfer occurred after the divergence of these two genera. Despite being of similar size and coding capacity, the level of synteny between L. oceanica and B. natans mtDNA is low, suggesting frequent rearrangements. Overall, our results suggest that chlorarachniophyte mtDNAs are more evolutionarily dynamic than their plastid counterparts.
Highlights
Endosymbiosis has played an important role in the generation of eukaryotic cellular diversity
Chlorarachniophyte algae belong to the eukaryotic supergroup Rhizaria, and together with cryptophyte algae, are an important lineage for the study of secondary endosymbiosis
Comparative genomics of nucleomorphs has revealed that a similar set of house keeping genes are retained in both chlorarachniophytes and cryptophytes, despite the independent origins of these endosymbiotically derived organelles[8,15,16,17,18,19,20,21]
Summary
Three protein genes (atp[8], rps[4] and rpl16) are absent from the Lotharella oceanica mitochondrial genome but present in Bigelowiella natans (Table 2). Given that these three proteins are generally necessary for energy production and translation in mitochondria, one explanation is that these three protein genes have moved to the L. oceanica nuclear genome by endosymbiotic gene transfer (EGT). The significant structural differences between the L. oceanica and B. natans mitochondrial genomes are especially interesting when compared to the plastid genomes of these two organisms Unlike their scrambled mtDNAs, gene order in the chlorarachniophyte plastid genomes that have been sequenced is nearly identical[21], yielding a single syntenic segment in a genome alignment (Fig. 4B). It is noteworthy that based on pulsed-field gel electrophoresis, Chlorarachnion reptans appears to contain an unusually large mtDNA (~180 kbp in size) compared with the other chlorarachniophyte strains[30] (Table 3)
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