Phylogenomic resolution of marine to freshwater dinoflagellate transitions.

Abstract

Dinoflagellates are an abundant and diverse group of protists that inhabit aquatic environments worldwide. They are characterized by numerous unique cellular and molecular traits, and have adapted to an unusually broad range of life strategies, including phototrophy, heterotrophy, parasitism, and all combinations of these. For most microbial groups, transitions from marine to freshwater environments are relatively rare, as changes in salinity are thought to lead to significant osmotic challenges that are difficult for the cell to overcome. Recent work has shown that dinoflagellates have overcome these challenges relatively often in evolutionary time, but because this is mostly based on single gene trees with low overall support, many of the relationships between freshwater and marine groups remain unresolved. Normally, phylogenomics could clarify such conclusions, but despite the recent surge in data, virtually no freshwater dinoflagellates have been characterized at the genome-wide level. Here, we generated 30 transcriptomes from cultures and single cells collected from freshwater environments to infer a robustly supported phylogenomic tree from 217 conserved genes, resolving at least seven transitions to freshwater in dinoflagellates. Mapping the distribution of ASVs from freshwater environmental samples onto this tree confirms these groups and identifies additional lineages where freshwater dinoflagellates likely remain unsampled. We also sampled two species of Durinskia, a genus of "dinotoms" with both marine and freshwater lineages containing Nitzschia-derived tertiary plastids. Ribosomal RNA phylogenies show that the host cells are closely related, but their endosymbionts are likely descended from two distantly-related freshwater Nitzschia species that were acquired in parallel and relatively recently.