Evolutionary recent dual obligatory symbiosis among adelgids indicates a transition between fungus and insect associated lifestyles

Abstract

ABSTRACTAdelgids (Insecta: Hemiptera: Adelgidae) form a small group of insects but harbor a surprisingly diverse set of bacteriocyte-associated endosymbionts, which suggest multiple replacement and acquisition of symbionts over evolutionary time. Specific pairs of symbionts have been associated with adelgid lineages specialized on different secondary host conifers. Using a metagenomic approach, we investigated the symbiosis of theAdelges laricis/tardusspecies complex containing betaproteobacterial (‘CandidatusVallotia tarda’) and gammaproteobacterial (‘CandidatusProfftia tarda’) symbionts. Genomic characteristics and metabolic pathway reconstructions revealed thatVallotiaandProfftiaare evolutionary young endosymbionts, which complement each other’s role in essential amino acid production. Phylogenomic analyses and a high level of genomic synteny indicate an origin of the betaproteobacterial symbiont from endosymbionts ofRhizopusfungi. This evolutionary transition was accompanied with substantial loss of functions related to transcription regulation, secondary metabolite production, bacterial defense mechanisms, host infection and manipulation. The transition from fungus to insect endosymbionts extends our current framework about evolutionary trajectories of host-associated microbes.