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

Abstract

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/tardus 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.

A highly divergent Wolbachia with a tiny genome in an insect-parasitic tylenchid nematode

“…Another possibility is that Wolbachia was perhaps acquired by Howardula nematodes relatively recently, from an as yet unknown lineage of hosts where it has been a symbiont for a long time. For example, some species of adelgids, insects that feed on conifer sap, have recently acquired obligate nutritional symbionts that are closely related to obligate bacterial symbionts of fungi [50,51]. It is interesting that the clade of fly parasitic Howardula nematodes and allies appears to contain mixtures of species that are free of symbionts, along with ones that have recently acquired putatively obligate symbionts.…”

Complex host/symbiont integration of a multi-partner symbiotic system in the eusocial aphid Ceratovacuna japonica

“…japonica aphid depends on Buchnera CJ and Arsenophonus CJ forming a co-obligate symbiosis. In several hemipteran insects, metabolic complementarity between co-symbionts has been observed (Husnik et al, 2013; Lamelas et al, 2011b; McCutcheon et al, 2009; Rao et al, 2015; Szabó et al, 2020; Wu et al, 2006). To determine if Buchnera CJ and Arsenophonus CJ form co-obligate associations with the host, we examined the genomic signature of metabolic complementarity by comparing the gene repertoires of these bacteria.…”

Subcellular niche segregation of co-obligate symbionts in whiteflies

“…In some co-obligate symbiotic systems in insects, each symbiont can complete the biosynthetic pathway of some essential nutrients, such as essential amino acids or vitamins, on its own or with host genes (13,(54)(55)(56)(57)(58). In other co-symbiotic systems, metabolic interdependence for some essential nutrients is present, wherein one of the symbionts possesses genes necessary for the first part of the biosynthetic pathway, and the other symbiont has genes necessary for the latter part of the pathway (10,12,13,(59)(60).…”