Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements

Abstract

BackgroundCryptophytes are an ecologically important group of algae comprised of phototrophic, heterotrophic and osmotrophic species. This lineage is of great interest to evolutionary biologists because their plastids are of red algal secondary endosymbiotic origin. Cryptophytes have a clear phylogenetic affinity to heterotrophic eukaryotes and possess four genomes: host-derived nuclear and mitochondrial genomes, and plastid and nucleomorph genomes of endosymbiotic origin.ResultsTo gain insight into cryptophyte mitochondrial genome evolution, we sequenced the mitochondrial DNAs of five species and performed a comparative analysis of seven genomes from the following cryptophyte genera: Chroomonas, Cryptomonas, Hemiselmis, Proteomonas, Rhodomonas, Storeatula and Teleaulax. The mitochondrial genomes were similar in terms of their general architecture, gene content and presence of a large repeat region. However, gene order was poorly conserved. Characteristic features of cryptophyte mtDNAs included large syntenic clusters resembling α-proteobacterial operons that encode bacteria-like rRNAs, tRNAs, and ribosomal protein genes. The cryptophyte mitochondrial genomes retain almost all genes found in many other eukaryotes including the nad, sdh, cox, cob, and atp genes, with the exception of sdh2 and atp3. In addition, gene cluster analysis showed that cryptophytes possess a gene order closely resembling the jakobid flagellates Jakoba and Reclinomonas. Interestingly, the cox1 gene of R. salina, T. amphioxeia, and Storeatula species was found to contain group II introns encoding a reverse transcriptase protein, as did the cob gene of Storeatula species CCMP1868.ConclusionsThese newly sequenced genomes increase the breadth of data available from algae and will aid in the identification of general trends in mitochondrial genome evolution. While most of the genomes were highly conserved, extensive gene arrangements have shuffled gene order, perhaps due to genome rearrangements associated with hairpin-containing mobile genetic elements, tRNAs with palindromic sequences, and tandem repeat sequences. The cox1 and cob gene sequences suggest that introns have recently been acquired during cryptophyte evolution. Comparison of phylogenetic trees based on plastid and mitochondrial genome data sets underscore the different evolutionary histories of the host and endosymbiont components of present-day cryptophytes.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4626-9) contains supplementary material, which is available to authorized users.

Recent advances in understanding mitochondrial genome diversity

“…The mitogenomes of Haptophyta 133 , Centrohelida 134 , and Cryptophyta 135 have been sequenced. (Sometimes these lineages have been grouped together within Hacrobia, although the monophyly of this group is highly controversial 136 .)…”

“…There are up to 12 unassigned ORFs. The mitogenomes of Cryptophyta are circular molecules ranging in size from 37 to 54 Kb 135 (Figure 2). The mitogenomes contain the same set of OXPHOS system protein-coding genes reported in Marophrys sp.…”

“…The genes cox1 and cob contain a group II intron in some species. Large syntenic blocks are conserved between species and a large repeat region is found 135 .…”

Mitochondrial Genomes of Hemiarma marina and Leucocryptos marina Revised the Evolution of Cytochrome c Maturation in Cryptista

“…For instance, no high-quality nuclear genome sequence is available for any cryptists except a cryptophyte Guillardia theta (Curtis et al, 2012) and a goniomonad Goniomonas avonlea (Cenci et al, 2018). Likewise, the complete mtDNAs are available from nine members of Cryptista, albeit seven out of the nine are cryptophytes (Hauth et al, 2005;Kim et al, 2008;Kim et al, 2018). Besides cryptophyte mtDNAs, Nishimura et al (2016) and Cenci et al (2018) reported the complete mtDNAs of P. bilix and G. avonlea, respectively.…”

The complete plastid genome of a marine microalgae Cryptophyceae sp. CCMP2293 (Cryptophyta)

“…Cryptophytes have strong adaptability to light and temperature and they become the dominant species in both winter and summer. Phototrophs of cryptophytes contain plastids with chlorophyll-a and -c, as well as phycobilins, as accessary pigments (Kim et al 2018). There are four genomes in cryptophyte cells: host-derived nuclear and mitochondrial genomes, and plastid and nucleomorph genomes of endosymbiotic origin (Douglas et al 1991).…”