Identification of Highly Divergent Diatom-Derived Chloroplasts in Dinoflagellates, Including a Description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae)

Abstract

Dinoflagellates are known to possess chloroplasts of multiple origins derived from a red alga, a green alga, haptophytes, or diatoms. The monophyletic "dinotoms" harbor a chloroplast of diatom origin, but their chloroplasts are polyphyletic belonging to one of four genera: Chaetoceros, Cyclotella, Discostella, or Nitzschia. It has been speculated that serial replacement of diatom-derived chloroplasts by other diatoms has caused this diversity of chloroplasts. Although previous work suggested that the endosymbionts of Nitzschia origin might not be monophyletic, this has not been seriously investigated. To infer the number of replacements of diatom-derived chloroplasts in dinotoms, we analyzed the phylogenetic affinities of 14 species of dinotoms based on the endosymbiotic rbcL gene and SSU rDNA, and the host SSU rDNA. Resultant phylogenetic trees revealed that six species of Nitzschia were taken up by eight marine dinoflagellate species. Our phylogenies also indicate that four separate diatom species belonging to three genera were incorporated into the five freshwater dinotoms. Particular attention was paid to two crucially closely related species, Durinskia capensis and a novel species, D. kwazulunatalensis, because they possess distantly related Nitzschia species. This study clarified that any of a total of at least 11 diatom species in five genera are employed as an endosymbiont by 14 dinotoms, which infers a more frequent replacement of endosymbionts in the world of dinotoms than previously envisaged.

The complete chloroplast and mitochondrial genomes of the diatomNitzschia palea(Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotomDurinskia baltica

“…The diatom that became the endosymbiont of the D. baltica (strain CSIRO CS‐38) is most closely related to the N. palea strain Spain C according to a phylogeny created by Yamada et al. () using the chloroplast rbc L marker. This is confirmed in the plastome and chondriome single gene phylogenies presented in this paper (Fig.…”

“…Indirect evidence that Nitzschia may have been the diatom genus incorporated into Durinskia was also noted by the presence of plastid plasmids in both genera (Imanian et al 2010). Most recently, Yamada et al (2017) analyzed rbcL and SSU rDNA sequences from 14 dinotoms and demonstrated a phylogenetic relationship of six marine dinotom endosymbionts to different Nitzschia species, showing this relationship has been initiated numerous times, independently. Several of the endosymbionts were resolved to the species level, including the dinotom D. baltica (strain CSIRO CS-38) which grouped with the Nitzschia palea strain "SpainC."…”

“…Most recently, Yamada et al. () analyzed rbc L and SSU rDNA sequences from 14 dinotoms and demonstrated a phylogenetic relationship of six marine dinotom endosymbionts to different Nitzschia species, showing this relationship has been initiated numerous times, independently. Several of the endosymbionts were resolved to the species level, including the dinotom D. baltica (strain CSIRO CS‐38) which grouped with the Nitzschia palea strain “SpainC.” The complete chloroplast genomes and fragments of the mitochondrial genomes of D. baltica and K. foliaceum have been sequenced (Imanian et al.…”

“…Considering plastome gene synteny, qualitative IGS similarities, and plastome-based phylogeny, there is a remarkable similarity between Durinskia baltica and Nitzschia palea. The diatom that became the endosymbiont of the D. baltica (strain CSIRO CS-38) is most closely related to the N. palea strain Spain C according to a phylogeny created by Yamada et al (2017) using the chloroplast rbcL marker. This is confirmed in the plastome and chondriome single gene phylogenies presented in this paper (Fig.…”

Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome

“…One possibility would be a serial endosymbiosis event deep in haptophyte evolutionary history, in which an ancient plastid derived from a pelagophyte/dictyochophyte ancestor was acquired by the haptophyte common ancestor, then replaced subsequently by a plastid of non-ochrophyte origin (Figure 10—figure supplement 2). This discrepancy, alongside others such as the presence of green algal genes in ochrophytes, bolsters the possibility that serial plastid endosymbiosis has been a widespread component of the evolution of CASH lineage plastids other than the dinoflagellates, in which it is a well established phenomenon (Dorrell and Howe, 2015; Yamada et al, 2017). Verifying this scenario, or its alternatives (such as lateral gene transfer from pelagophyte or dictyochophyte algae into the algal ancestors of the haptophyte plastid) rests on identifying the exact origin of the current haptophyte plastid genome, and in particular demonstrating that the haptophyte plastid genome originates from within (rather than forms a sister-group to) a major lineage of eukaryotic algae other than ochrophytes (Figure 10—figure supplement 2).…”