Evolutionary Dynamics of Cryptophyte Plastid Genomes

Abstract

Cryptophytes are an ecologically important group of largely photosynthetic unicellular eukaryotes. This lineage is of great interest to evolutionary biologists because their plastids are of red algal secondary endosymbiotic origin and the host cell retains four different genomes (host nuclear, mitochondrial, plastid, and red algal nucleomorph). Here, we report a comparative analysis of plastid genomes from six representative cryptophyte genera. Four newly sequenced cryptophyte plastid genomes of Chroomonas mesostigmatica, Ch. placoidea, Cryptomonas curvata, and Storeatula sp. CCMP1868 share a number of features including synteny and gene content with the previously sequenced genomes of Cryptomonas paramecium, Rhodomonas salina, Teleaulax amphioxeia, and Guillardia theta. Our analysis of these plastid genomes reveals examples of gene loss and intron insertion. In particular, the chlB/chlL/chlN genes, which encode light-independent (dark active) protochlorophyllide oxidoreductase (LIPOR) proteins have undergone recent gene loss and pseudogenization in cryptophytes. Comparison of phylogenetic trees based on plastid and nuclear genome data sets show the introduction, via secondary endosymbiosis, of a red algal derived plastid in a lineage of chlorophyll-c containing algae. This event was followed by additional rounds of eukaryotic endosymbioses that spread the red lineage plastid to diverse groups such as haptophytes and stramenopiles.

Keywords: cryptophyte; horizontal gene transfer; plastid genome.

Fig. 1.

—Circular map of the plastid genome of Cryptomonas curvata FBC300012D showing nine syntenic regions. (A) The gene content and arrangement of the photosynthetic cryptophyte genomes are identical with the exception of the nine syntenic regions shown as (A–I). The protein coding genes, rRNA and tRNA genes are labeled inside or outside of the circle. The genes are color-coded according to the functional categories in the index. (B) Linear form of the nine syntenic regions indicates the lineage-specific gene losses and intron insertions among cryptophytes.

Fig. 2.

—Distribution of 11 patchily distributed genes in the major photosynthetic eukaryotic groups. These genes show outright gene losses, pseudogenes, and intron insertions. The cladogram was built using a concatenated data set of 88 plastid genes (fig. 3 and supplementary table S1, Supplementary Material online). The 11 target genes are color-coded: purple = three LIPOR genes, yellow = dnaX gene, and dark blue = dnaK, groEL, ftsH, minD/E, hlpA, and dnaB genes. The open white circles indicate gene absence in plastid genomes.

Fig. 3.

—Phylogenetic tree of cryptophyte plastids and those of other photosynthetic eukaryotes. This tree was constructed using a data set of 88 concatenated proteins (16,878 amino acids). The numbers on each node represent RAxML bootstrap values (left) and ultrafast bootstrap approximation (UFBoot) using IQ-Tree (right). The scale bar indicates the number of substitutions/site.

Fig. 4.

—Secondary endosymbiotic origin of red alga-derived plastids and the nuclear multigene tree of eukaryotes. (A) The plastid-genome based tree of algae with the red arrow (marked with “S”) showing the putative single origin of the red alga-derived plastid in chlorophyll-c containing algae. (B) The nuclear multigene tree of life showing the putative relationships of chlorophyll-c containing algae in the context of nonphotosynthetic lineages. A possible explanation for the conflict in topology between the plastid and nuclear gene trees is that there were multiple independent red algal secondary endosymbioses in the photosynthetic lineages (either two events [marked with “B” and green arrows] or three events [marked with “C” and blue arrows]). A more likely scenario is that there was a single red algal secondary endosymbiosis (perhaps in the cryptophyte ancestor), followed by serial eukaryotic endosymbioses involving chlorophyll-c lineages that spread the plastid to other groups (marked with “Se” and magenta arrows).