Adelgids (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 the Adelges laricis/Adelgestardus species complex containing betaproteobacterial
("Candidatus Vallotia tarda") and gammaproteobacterial ("Candidatus Profftia tarda")
symbionts. Genomic characteristics and metabolic pathway reconstructions revealed
that Vallotia and Profftia are 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 of Rhizopus fungi. 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.