Host-specific co-evolution likely driven by diet in Buchnera aphidicola

Abstract

Background Russian wheat aphid (Diuraphis noxia Kurd.) is a severe pest to wheat, and even though resistance varieties are available to curb this pest, they are becoming obsolete with the development of new virulent aphid populations. Unlike many other aphids, D noxia only harbours a single endosymbiont, Buchnera aphidicola. Considering the importance of Buchnera, this study aimed to elucidate commonalities and dissimilarities between various hosts, to better understand its distinctiveness within its symbiotic relationship with D. noxia. To do so, the genome of the D. noxia’s Buchnera was assembled and compared to those of other aphid species that feed on diverse host species.Results The overall importance of several features such as gene length and percentage GC content was found to be critical for the maintenance of Buchnera genes when compared to their closest free-living relative, Escherichia coli. Buchnera protein coding genes were found to have percentage GC contents that tended towards a mean of ~ 26% which had strong correlation to their identity to their E. coli homologs. Several SNPs were identified between different aphid populations and multiple isolates of Buchnera were confirmed in single aphids.Conclusions Establishing the strong correlation of percentage GC content of protein coding genes and gene identity will allow for identifying which genes will be lost in the continually shrinking Buchnera genome. This is also the first report of a parthenogenically reproducing aphid that hosts multiple Buchnera strains in a single aphid, raising questions regarding the benefits of maintaining multiple strains. We also found preliminary evidence for post-transcriptional regulation of Buchnera genes in the form of polyadenylation.

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

“…Our findings indicate that multiple genetically different strains of Buchnera may coexist as a ‘population’ within their clonal M. persicae host. This parallels very recent work that has also identified coexisting Buchnera strains in four different clonal lineages of Russian wheat aphid, Diuraphis noxia (Burger, Nicolis, & Botha, 2023). Limited plasticity of Buchnera ’s genetic regulatory capacity (Moran et al, 2003; Neiers, Saliou, Briand, & Robichon, 2021; Wilcox, Dunbar, Wolfinger, & Moran, 2003) suggests that physiological effects of Buchnera on their aphid host is likely via genetically encoded variants.…”

“…Our findings indicate that multiple genetically different strains of Buchnera may coexist as a ‘population’ within their clonal M. persicae host. This parallels very recent genomic work that has also identified coexisting Buchnera strains in four different clonal lineages of Russian wheat aphid, Diuraphis noxia (Burger, Nicolis, & Botha, 2023). Modern whole-genome sequencing may thus provide power to unearth previously unappreciated within and among clonal lineage variation required for asexual organisms to evolve (Loxdale & Lushai, 2003), but this has yet to be fully realized.…”