Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte?

Abstract

Algae with secondary plastids of a red algal origin, such as ochrophytes (photosynthetic stramenopiles), are diverse and ecologically important, yet their evolutionary history remains controversial. We sequenced plastid genomes of two ochrophytes, Ochromonas sp. CCMP1393 (Chrysophyceae) and Trachydiscus minutus (Eustigmatophyceae). A shared split of the clpC gene as well as phylogenomic analyses of concatenated protein sequences demonstrated that chrysophytes and eustigmatophytes form a clade, the Limnista, exhibiting an unexpectedly elevated rate of plastid gene evolution. Our analyses also indicate that the root of the ochrophyte phylogeny falls between the recently redefined Khakista and Phaeista assemblages. Taking advantage of the expanded sampling of plastid genome sequences, we revisited the phylogenetic position of the plastid of Vitrella brassicaformis, a member of Alveolata with the least derived plastid genome known for the whole group. The results varied depending on the dataset and phylogenetic method employed, but suggested that the Vitrella plastids emerged from a deep ochrophyte lineage rather than being derived vertically from a hypothetical plastid-bearing common ancestor of alveolates and stramenopiles. Thus, we hypothesize that the plastid in Vitrella, and potentially in other alveolates, may have been acquired by an endosymbiosis of an early ochrophyte.

Figure 1. Plastid phylogeny inferred from protein sequences encoded by 34 slowly-evolving conserved plastid genes (dataset SG, 14,699 aa positions).

(A) Maximum-likelihood tree (RAxML, GTRGAMMA model); only the “chromalveolate” subtree is shown for simplicity. Thick branches received 100% bootstrap support, otherwise the bootstrap support values are indicated by numbers when higher than 50%. (B) PhyloBayes tree inferred using the CAT-GTR model. Thick branches were supported by 1.00 posterior probability and 100% bootstrap support values from the ML analyses, otherwise posterior probabilities / bootstrap support values are indicated by numbers when higher than 0.90 / 50%; “d.t.” means that the respective bipartition does not exist in the ML tree.

Figure 2. The phylogenetic position of the Vitrella brassicaformis plastid.

The trees were inferred from a concatenated matrix of 34 slowly-evolving conserved plastid genes (dataset SG, 14,699 aa positions) excluding the rapidly evolving genome of Karlodinium veneficum. (A) Maximum-likelihood tree (RAxML, GTRGAMMA model); only the “chromalveolate” subtree is shown for simplicity. (B) PhyloBayes tree inferred using the CAT-GTR model. The convention for indicating branch support values is the same as in Fig. 1.