The Large Mitochondrial Genome ofSymbiodinium minutumReveals Conserved Noncoding Sequences between Dinoflagellates and Apicomplexans

Abstract

Even though mitochondrial genomes, which characterize eukaryotic cells, were first discovered more than 50 years ago, mitochondrial genomics remains an important topic in molecular biology and genome sciences. The Phylum Alveolata comprises three major groups (ciliates, apicomplexans, and dinoflagellates), the mitochondrial genomes of which have diverged widely. Even though the gene content of dinoflagellate mitochondrial genomes is reportedly comparable to that of apicomplexans, the highly fragmented and rearranged genome structures of dinoflagellates have frustrated whole genomic analysis. Consequently, noncoding sequences and gene arrangements of dinoflagellate mitochondrial genomes have not been well characterized. Here we report that the continuous assembled genome (∼326 kb) of the dinoflagellate, Symbiodinium minutum, is AT-rich (∼64.3%) and that it contains three protein-coding genes. Based upon in silico analysis, the remaining 99% of the genome comprises transcriptomic noncoding sequences. RNA edited sites and unique, possible start and stop codons clarify conserved regions among dinoflagellates. Our massive transcriptome analysis shows that almost all regions of the genome are transcribed, including 27 possible fragmented ribosomal RNA genes and 12 uncharacterized small RNAs that are similar to mitochondrial RNA genes of the malarial parasite, Plasmodium falciparum. Gene map comparisons show that gene order is only slightly conserved between S. minutum and P. falciparum. However, small RNAs and intergenic sequences share sequence similarities with P. falciparum, suggesting that the function of noncoding sequences has been preserved despite development of very different genome structures.

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

“…They encode the same set of three divergent protein-coding genes: cob (cytochrome b), cox1 (cytochrome c oxidase subunit 1), and cox3 (cytochrome c oxidase subunit 3), two highly fragmented rRNA genes for large (LSU) and small (SSU) ribosomal subunits, as well as some uncharacterized small RNA fragments (Shoguchi et al 2015). Compared to the mitogenome of their closest known Alveolata relative, Acavomonas peruviana, the myzozoan mitogenomes must have lost 45 genes ( Figure 1; Janouskovec et al 2013).…”

“…The mitogenome size of Symbiodinium minutum, a reef-building coral endosymbiont, amounts to 326 kb, including mostly (99%) noncoding sequences. It is more than 50 times the size of the Plasmodium falciparum mitogenome (an apicomplexan that causes malaria), and 20 times the size of ours (Ji et al 1996;Shoguchi et al 2015). Still, the dinoflagellate mitochondrial genomes are smaller than the megabase-sized mitogenomes of some plants, e.g.…”

“…In dinoflagellates, genes were amplified to numerous copies, which resulted in an increase in their genome size amounting e.g. to 300 kb in Symbiodinium (Shoguchi et al 2015). In these protists and sister lineages, various interesting molecular mechanism evolved, such as: translational frameshifting, the addition of 8-9 uridine caps at 5 0 end of mRNAs, trans-splicing, and RNA editing (Flegontov & Luke s 2012).…”

“…It is assumed that universal start (ATG) and stop (TAA) codons, still present in apicomplexans, were independently lost in chromerids and the perkinsid-dinoflagellate branch. Given this model, the presence of TAA at the cox3 gene in Hematodinium (Jackson et al 2012) as well as ATG and TAA at cob in Symbiodinium (Shoguchi et al 2015) implies that these codons may have originated de novo. Alternatively, these codons might represent an ancestral state and many alveolates (Perkinsus, Oxyrrhis, and other dinoflagellates) lost these codons independently.…”

“…in cox1, by causing a kind of 'sliding' movement of the ribosome that prematurely terminates translation (Koutmou et al 2015). Only the cob gene, in S. minutum at least, has both canonical start and stop codons (Shoguchi et al 2015). This means that stop codons are still used in dinoflagellates and have not been, for example, reassigned to other amino acids.…”