All essential endosymbionts of the ciliate Euplotes are cyclically replaced

Abstract

Symbiotic systems vary in the degree to which the partners are bound to each other1. At one extreme, there are intracellular endosymbionts in mutually obligate relationships with their host, often interpreted as mutualistic. The symbiosis between the betaproteobacterium Polynucleobacter and the ciliate Euplotes (clade B) challenges this view2: although freshwater Euplotes species long ago became dependent on endosymbionts, the many extant Polynucleobacter lineages they harbour arose recently and in parallel from different free-living ancestors2. The host requires the endosymbionts for reproduction and survival3, but each newly established symbiont is ultimately driven to extinction in a cycle of establishment, degeneration, and replacement. Similar replacement events have been observed in sap-feeding insects4-6, a model for bacteria-eukaryote symbioses7, but usually only affect a small subset of the host populations. Most insects retain an ancient coevolving symbiont, suggesting that long-term mutualism and permanent integration remain the rule and symbiont turnovers are mere evolutionary side-stories. Here we show that this is not the case for Euplotes. We examined all known essential Euplotes symbionts and found that none are ancient or coevolving; rather, all are recently established and continuously replaced over relatively short evolutionary time spans, making the symbiosis ancient for the host but not for any bacterial lineage.