Highly reduced genomes of protist endosymbionts show evolutionary convergence

Abstract

Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1–4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. However, eukaryotic microbes, or protists, also harbor diverse bacterial endosymbionts, but their genome reduction and functional relationships with their more diverse hosts are largely unexplored [5–7]. We sequenced the genomes of four bacterial endosymbionts from three species of diplonemids, poorly-studied but abundant and diverse heterotrophic protists [8–10]. The endosymbionts come from two intracellular families from different orders, Rickettsiaceae and Holosporaceae, that have invaded diplonemids multiple times, and their genomes have converged on an extremely small size (605–632 kbp), similar gene content (e.g., metabolite transporters and secretion systems), and reduced metabolic potential (e.g., loss of energy metabolism). These characteristics are generally found in both families, but the diplonemid endosymbionts have evolved greater extremes in parallel. Their modified type VI secretion systems are likely involved in the manipulation of host metabolism (e.g., interactions with host mitochondria) or defense against bacterial infections, although their similar effector/immunity proteins may also allow for co-occurring Holosporaceae species in one diplonemid host. Finally, modified cellular machinery like ATP synthase without oxidative phosphorylation and reduced flagella present in both diplonemid endosymbionts and nutritional animal endosymbionts indicates that intracellular mechanisms have converged in bacterial endosymbionts with various functions and from different eukaryotic hosts across the tree of life.