Chaos and repetition in algal evolution: A Chrysophyceae eco-genomic framework

Abstract

The Chrysophyceae are an algal class that, within relatively short evolutionary distances, have repeatedly adopted multiple trophic strategies (photoautotrophy, mixotrophy, heterotrophy) and are ubiquitous across marine, freshwater and cryosphere ecosystems. Historical understanding of marine chrysophytes has lagged behind that of freshwater taxa, limiting our ability to identify what genes determine their cellular and ecosystem function. We leverage new transcriptomes, meta-genomes and computational predictions to reveal the functional, genetic and eco-physiological diversity of Chrysophyceae, including newly documented marine groups. We show that their common ancestor was likely a marine mixotroph, with multiple independent colonizations of freshwater and cryospheres, and evolution of photoautotrophic and heterotrophic life-strategies. We identify characteristic biogeographical distributions for different Chrysophyceae orders, including new ones linking marine and freshwater cryospheres. We document convergent gene losses relating to cryotolerance, photosynthesis, and phagocytosis, including novel families widely spread across the algal tree of life. We map meta-gene distributions of marker genes and impute a latitudinal shift in Chrysophyceae trophic strategy, with photoautotrophy predominant in polar oceans and heterotrophy in oligotrophic tropical waters. Our study identifies new gene markers that may be determinant of lifestyle shifts across the algal tree of life and reveals probable responses of marine chrysophytes to climate change.