Inferior Caballeronia symbiont lacks conserved symbiosis genes.

Abstract

Pentatomomorphan bugs can form symbiotic associations with bacteria belonging to the supergenus Burkholderia sensu lato. This relationship has become a model for understanding environmental symbiont acquisition. Host insects can utilize various symbiont strains from across Burkholderia sensu lato; however, host colonization success and benefits conferred vary by bacterial clade. Therefore, we conducted a meta-analysis aimed at identifying candidate genes that underpin beneficial symbioses within this system. We scanned the entire Burkholderiaceae family for the presence of 17 colonization-associated genes, as well as 88 candidate genes that are differentially expressed during symbiosis. There was no difference in the distribution of the 17 colonization-associated genes between symbiotic (Caballeronia and insect-associated plant beneficial and environmental clade) and non-symbiotic lineages; however, there was a higher prevalence of the 88 candidate genes in the insect symbiont lineages. We subsequently analysed the genomes of nine symbiotic Caballeronia species that confer varying fitness benefits to their insect hosts. One symbiont species was significantly worse, one was significantly better and the remaining seven were intermediate in terms of conferred host fitness benefits. We found that species possessing a higher number of the candidate genes conferred faster host development time. Furthermore, we identified two candidate genes that were missing in the least beneficial species but present in the other eight, suggesting that these genes may be important in modulating symbiont quality. Our study suggests that the mechanisms required for host colonization are broadly distributed across Burkholderiaceae, but the genes that determine symbiont quality are more prevalent in insect-associated species. This work helps to identify genes that influence this highly specialized yet diverse symbiosis between Pentatomomorphan insects and Burkholderiaceae bacteria.