A stochastic ratchet during genome streamlining can commit insect endosymbionts to a parasitic or mutualistic fate

Abstract

Many arthropods, including insects, harbor endosymbiotic bacteria. As bacteria transitioned to live inside host cells, free-living bacterial ancestors of endosymbionts reduced their genomes in a process known as streamlining. Contemporary endosymbioses represent at least two distinct life strategies: endosymbionts either become unilaterally dependent on host-derived resources (uni-obligate) or enter bidirectionally obligate mutualistic relationships (bi-obligate endosymbiosis). It is an open question whether these paths taken by free-living bacteria can be sequential, or alternatively, if commitment takes place early, making these strategies mutually exclusive. In this study, we quantified metabolic capacity of different endosymbionts to contextualize genome streamlining in terms of organismal function. We show that uni-obligate endosymbionts of insects have lost substantial parts of their metabolic capacity that are present both in free-living bacteria and bi-obligate endosymbionts. On the contrary, genomes of uni-obligate endosymbionts contain more genes which can be attributed to scavenging host resources. In sum, we challenge the existing notion that bi-obligate endosymbionts have emerged from uni-obligate ones, and rather, propose a stochastic ratchet model: in early stages of endosymbiosis, bacteria get locked into either a more mutualistic or more parasitic relationship with the host depending on the first losses during streamlining.