A Comparative Analysis of Mitochondrial Genomes in Eustigmatophyte Algae

Abstract

Eustigmatophyceae (Ochrophyta, Stramenopiles) is a small algal group with species of the genus Nannochloropsis being its best studied representatives. Nuclear and organellar genomes have been recently sequenced for several Nannochloropsis spp., but phylogenetically wider genomic studies are missing for eustigmatophytes. We sequenced mitochondrial genomes (mitogenomes) of three species representing most major eustigmatophyte lineages, Monodopsis sp. MarTras21, Vischeria sp. CAUP Q 202 and Trachydiscus minutus, and carried out their comparative analysis in the context of available data from Nannochloropsis and other stramenopiles, revealing a number of noticeable findings. First, mitogenomes of most eustigmatophytes are highly collinear and similar in the gene content, but extensive rearrangements and loss of three otherwise ubiquitous genes happened in the Vischeria lineage; this correlates with an accelerated evolution of mitochondrial gene sequences in this lineage. Second, eustigmatophytes appear to be the only ochrophyte group with the Atp1 protein encoded by the mitogenome. Third, eustigmatophyte mitogenomes uniquely share a truncated nad11 gene encoding only the C-terminal part of the Nad11 protein, while the N-terminal part is encoded by a separate gene in the nuclear genome. Fourth, UGA as a termination codon and the cognate release factor mRF2 were lost from mitochondria independently by the Nannochloropsis and T. minutus lineages. Finally, the rps3 gene in the mitogenome of Vischeria sp. is interrupted by the UAG codon, but the genome includes a gene for an unusual tRNA with an extended anticodon loop that we speculate may serve as a suppressor tRNA to properly decode the rps3 gene.

Recent advances in understanding mitochondrial genome diversity

“…Within Straminopiles (or Heterokonta), the size and gene content of the mitogenomes of the main groups are generally conserved (Figure 2). Several mitogenomes of Ochrophyta algae from families Chrysophyceae 116 , Phaeophyceae 117 , Eustigmatophyceae 118 , and Bacillariophyceae (diatoms 119 ) have been sequenced. The circular genomes normally vary in size between 34 and 77 Kb, depending on intervening sequences of variable length.…”

“…It is a circular molecule of 43 Kb, which has the same gene content as Amoebozoa mitogenomes 122 . Remarkably, the nad11 gene in many Heterokonta is split into two fragments; in several groups (for example, all Eustigmatophyceae, some Bacillariophyceae, and some Bygira), one of the fragments is relocated to the nuclear genome 118 . The mitogenomes of Blastocystis are exceptional within Heterokonta as the species of this genus have mitochondrion-related organelles instead of true mitochondria 123 .…”

The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite

“…As to the first question, correlating the occurrence of the operon with the eustigmatophyte phylogeny [10,14] needs to be considered. Vischeria and Monodopsis both belong to the order Eustigmatales, whereas the second major eustigmatophyte group, the clade Goniochloridales represented by the plastome sequence from T. minutus , lacks the ebo operon (figure 1).…”

“…CAUP Q 202 and Monodopsis sp. MarTras21 was described previously [14]. Briefly, 454 and Illumina reads (in the case of Vischeria sp.)…”

“…For the genera Nannochloropsis and Microchloropsis , only the type species are shown for simplicity, although plastomes have been sequenced for a number of other closely related species or strains. The topology of the tree reflects a robustly resolved phylogeny based on the 18S rRNA gene [14]. Evolutionary events impacting the gene content of eustigmatophyte plastid genomes are mapped onto the tree based on the most parsimonious interpretation of the pattern of the gene presence/absence (provided in the electronic supplementary material, table S1).…”