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

Gitta Szabó,Elena Rebecca Toenshoff,Frederik Schulz,Matthias Horn,Alejandro Manzano-Marín

doi:10.1038/s41396-021-01056-z

Gitta Szabó, Elena Rebecca Toenshoff + Show 3 more

Open Access

https://doi.org/10.1038/s41396-021-01056-z

Copy DOI

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/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.

Highlights

Most plant sap-feeding insects harbor bacterial endosymbionts, which are of great importance in their host ecology and serve as a model for studying microbe–host relationships and genome evolution of host-restricted bacteria [1,2,3]
Phylogenetic analysis of 45 single-copy proteins demonstrated that Profftia opens up a novel insect symbiont lineage most similar to Hafnia species and an isolate from the human gastrointestinal tract within the Hafniaceae, which has been recently designated as a distinct family within the Enterobacteriales [57] (Fig. S2)
Given the well-supported phylogenetic positioning of “Candidatus Vallotia tarda” nested within a clade formed by Mycetohabitans species, we propose the transfer of “Candidatus Vallotia tarda” to the Mycetohabitans genus, as “Candidatus Mycetohabitans vallotii”

Summary

Introduction

Most plant sap-feeding insects harbor bacterial endosymbionts, which are of great importance in their host ecology and serve as a model for studying microbe–host relationships and genome evolution of host-restricted bacteria [1,2,3]. How these insect–bacteria partnerships arise is still poorly understood, because the precursor of the endosymbionts can rarely be identified [4,5,6]. Other adelgids reproduce asexually on either of the host genera [8]

Methods

Results

Conclusion