Multiple plastid losses within photosynthetic stramenopiles revealed by comprehensive phylogenomics.

Abstract

Ochrophyta is a vast and morphologically diverse group of algae with complex plastids, including familiar taxa with fundamental ecological importance (diatoms or kelp) and a wealth of lesser-known and obscure organisms. The sheer diversity of ochrophytes poses a challenge for reconstructing their phylogeny, with major gaps in sampling and an unsettled placement of particular taxa yet to be tackled. We sequenced transcriptomes from 25 strategically selected representatives and used these data to build the most taxonomically comprehensive ochrophyte-centered phylogenomic supermatrix to date. We employed a combination of approaches to reconstruct and critically evaluate the relationships among ochrophytes. While generally congruent with previous analyses, the updated ochrophyte phylogenomic tree resolved the position of several taxa with previously uncertain placement and supported a redefinition of the classes Picophagea and Synchromophyceae. Our results indicated that the heterotrophic, plastid-lacking heliozoan Actinophrys sol is not a sister lineage of ochrophytes, as proposed recently, but rather phylogenetically nested among them, implying that it lacks a plastid due to loss. In addition, we found the heterotrophic ochrophyte Picophagus flagellatus to lack all hallmark plastid genes yet to exhibit mitochondrial proteins that seem to be genetic footprints of a lost plastid organelle. We thus document, for the first time, plastid loss in two separate ochrophyte lineages. Furthermore, by exploring eDNA data, we enrich the ochrophyte phylogenetic tree by identifying five novel uncultured class-level lineages. Altogether, our study provides a new framework for reconstructing trait evolution in ochrophytes and demonstrates that plastid loss is more common than previously thought.