Elucidation of host and symbiont contributions to peptidoglycan metabolism based on comparative genomics of eight aphid subfamilies and their Buchnera

Abstract

Pea aphids (Acyrthosiphon pisum) are insects containing genes of bacterial origin with putative functions in peptidoglycan (PGN) metabolism. Of these, rlpA1-5, amiD, and ldcA are highly expressed in bacteriocytes, specialized aphid cells that harbor the obligate bacterial symbiont Buchnera aphidicola, required for amino acid supplementation of the host’s nutrient-poor diet. Despite genome reduction associated with endosymbiosis, pea aphid Buchnera retains genes for the synthesis of PGN while Buchnera of many other aphid species partially or completely lack these genes. To explore the evolution of aphid horizontally-transferred genes (HTGs) and to elucidate how host and symbiont genes contribute to PGN production, we sequenced genomes from four deeply branching lineages, such that paired aphid and Buchnera genomes are now available for 17 species representing eight subfamilies. We identified all host and symbiont genes putatively involved in PGN metabolism. Phylogenetic analyses indicate that each HTG family was present in the aphid shared ancestor, but that each underwent a unique pattern of gene loss or duplication in descendant lineages. While four aphid rlpA gene subfamilies show no relation to symbiont PGN gene repertoire, the loss of aphid amiD and ldcA HTGs coincides with the loss of symbiont PGN metabolism genes. In particular, the coincident loss of host amiD and symbiont murCEF in tribe Aphidini, in contrast to tribe Macrosiphini, suggests either 1) functional linkage between these host and symbiont genes, or 2) Aphidini has lost functional PGN synthesis and other retained PGN pathway genes are non-functional. To test these hypotheses experimentally, we used cell-wall labeling methods involving a d-alanine probe and found that both Macrosiphini and Aphidini retain Buchnera PGN synthesis. Our results imply that compensatory adaptations can preserve PGN synthesis despite the loss of some genes considered essential for this pathway, highlighting the importance of the cell wall in these symbioses.

Comparative transcriptomics of aphid species that diverged > 22 MYA reveals genes that are important for the maintenance of their symbiosis

“…Nakabachi et al 37 demonstrated that RplA is synthesized as a protein in the maternal bacteriocyte and is transported into Buchnera cells. This horizontally transmitted gene is hypothesized to produce lytic translgycosylase for Buchnera cell wall remodeling and is largely omnipresent in Aphidoidea unlike other horizontally transferred genes that were lost in certain aphid lineages 38 .…”

‘Drifting’Buchneragenomes track the microevolutionary trajectories of their aphid hosts

“…D-amino acids are used to synthesize peptidoglycan and build the cell wall. Buchnera from the aphid tribe Macrosiphini (which includes M. persicae) contribute to building their own cell wall (Smith et al, 2022).…”

Cuticle supplementation and nitrogen recycling by a dual bacterial symbiosis in a family of xylophagous beetles (Coleoptera: Bostrichidae)

“…S4). Especially the pathways for synthesis of the cell envelopes are intriguing, as cell wall synthesis has been demonstrated to be complemented and controlled by host encoded genes and inter-symbiont exchange of metabolites in hemipteran symbionts (Bublitz et al, 2019; Smith et al, 2021, 2022).…”