The mitochondrial genomes of the glaucophytes Gloeochaete wittrockiana and Cyanoptyche gloeocystis: multilocus phylogenetics suggests a monophyletic archaeplastida

Abstract

A significant limitation when testing the putative single origin of primary plastids and the monophyly of the Archaeplastida supergroup, comprised of the red algae, viridiplants, and glaucophytes, is the scarce nuclear and organellar genome data available from the latter lineage. The Glaucophyta are a key algal group when investigating the origin and early diversification of photosynthetic eukaryotes. However, so far only the plastid and mitochondrial genomes of the glaucophytes Cyanophora paradoxa (strain CCMP 329) and Glaucocystis nostochinearum (strain UTEX 64) have been completely sequenced. Here, we present the complete mitochondrial genomes of Gloeochaete wittrockiana SAG 46.84 (36.05 kb; 33 protein-coding genes, 6 unidentified open reading frames [ORFs], and 28 transfer RNAs [tRNAs]) and Cyanoptyche gloeocystis SAG 4.97 (33.24 kb; 33 protein-coding genes, 6 unidentified ORFs, and 26 tRNAs), which represent two genera distantly related to the "well-known" Cyanophora and Glaucocystis. The mitochondrial gene repertoire of the four glaucophyte species is highly conserved, whereas the gene order shows considerable variation. Phylogenetic analyses of 14 mitochondrial genes from representative taxa from the major eukaryotic supergroups, here including novel sequences from the glaucophytes Cyanophora tetracyanea (strain NIES-764) and Cyanophora biloba (strain UTEX LB 2766), recover a clade uniting the three Archaeplastida lineages; this recovery is dependent on our novel glaucophyte data, demonstrating the importance of greater taxon sampling within the glaucophytes.

Keywords: Cyanophora; Plantae; glaucophyta; phylogenetics.

Fig. 1.—

Gloeochaete wittrockiana and Cyanoptyche gloeocystis mtDNAs and cumulative GC-skew plots. (A) Circular gene maps of Glo. wittrockiana (strain SAG 46.84) and Cyanopt. gloeocystis (strain SAG 4.97) mitochondrial genomes. Colored bars identify types of genes/ORFs: rRNAs (red), tRNA (blue), ribosomal proteins (purple), complex I (yellow), complex II (pink), complex III and IV (dark gray), complex V (green), uORFs (orange). Red arrowheads indicate overlaps between genes. (B) Cumulative GC-skew plots for Glo. wittrockiana and Cyanopt. gloeocystis mtDNAs. y axis: cumulative GC skew, x axis: position in the genome.

Fig. 2.—

Putative rrn5 sequence from Cyanoptyche gloeocystis mtDNA, aligned with rrn5 sequences from C. paradoxa and G. nostochinearum (A); putative secondary structure of Cyanopt. gloeocystis rrn5 (B). The inset shows the proposed structure of the E. coli rrn5 for reference. Helices are shown by Roman numerals (I–V), and single-stranded regions are shown by upper case letters (A–D).

Fig. 3.—

Gene rearrangements in glaucophyte mtDNAs. Individual genes are shown as grayscale rectangles, with genome organization and gene strand location shown below. Black lines connect genes found in each mtDNA (tRNA genes excluded). Rectangles with no lines represent unique ORFs, or genes not found in all taxa. C.g., Cyanopt. gloeocystis; G.w., Glo. wittrockiania; C.p., C. paradoxa; G.n., G. nostochinearum.

Fig. 4.—

Phylogenetic analysis of 14 mitochondrial genes. ML phylogenetic tree estimated from conceptual translations (A) and nucleotide sequences (B) of atp6, atp9, cob, cox1, cox2, cox3, nad1, nad2, nad3, nad4, nad4L, nad5, nad6, and nad7. Numbers above and below branches represent Bayesian PP and RAxML BS proportions, respectively. Thick branches are supported by PP and BS values greater than 95. Branches without PP values were only recovered in the ML analysis. Branch lengths are proportional to the number of substitutions per site.