Bacteria Associated with Russian Wheat Aphid (Diuraphis noxia) Enhance Aphid Virulence to Wheat

Abstract

Phenotypic responses to biotic stresses are often studied as the interactions between two species; however, in the phytobiome, these responses frequently result from complex interactions involving several organisms. Here, we show that variation in chlorosis caused by Russian wheat aphid (Diuraphis noxia) feeding is determined, in part, by aphid-associated bacteria. Proteomic analysis of fluids injected into a sterile medium by the aphid during feeding indicate that 99% of the proteins are of bacterial origin. Of these, the greatest proportion are produced by bacteria in the order Enterobacteriales. Bacteria from five genera in four families that have the capacity to produce these proteins were isolated directly from aphids as well as from wheat leaves only after D. noxia feeding. By themselves or in combination, these bacteria were not virulent to wheat, even at high inoculum levels. Metagenomic analysis showed that the same five D. noxia-associated genera dominated the non-Buchnera component of the aphid microbiome, and that representation of these genera was reduced in aphids from colonies established after isolation of newborn nymphs from their mothers prior to feeding (isolated aphids). Isolation or treatment with antibiotics reduced bacterial numbers, and these aphids caused less feeding damage on wheat than non-isolated or non-antibiotic-treated aphids. Our data show that bacterial proteins are a significant component of Russian wheat aphid saliva, that the bacteria producing these proteins are associated with aphids and plants fed upon by aphids, and that these aphid-associated bacteria facilitate aphid virulence to wheat.

Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid

“…Given the fact that insect microbiomes are partly acquired from their host's environment (Hannula, Zhu, Heinen, & Bezemer, ; Jones et al, ), it cannot be excluded that the strains investigated may not be representative for what the insects would carry in more natural situations. However, most of the bacteria investigated here were previously found in association with aphids, parasitoids and their environment (Grigorescu et al, ; Leroy, Sabri, Heuskin, et al, ; Luna et al, ), reinforcing the robustness of our results.…”

“…Strains were isolated from diverse sources sampled in greenhouses or a laboratory environment, including unparasitized aphids, aphid mummies, honeydew and Aphidius and Dendrocerus female adults. Studied strains represented a phylogenetically diverse collection of bacteria belonging to Actinobacteria, Firmicutes and Proteobacteria, which are typically associated with insects and insect‐derived products (Engel & Moran, ; Grigorescu et al, ; Leroy, Sabri, Heuskin, et al, ; Luna et al, ). Further details on the isolation source (e.g.…”

Inside out: microbiota dynamics during host-plant adaptation of whiteflies

“…For example, the deposition on the leaf surface of a pathogenic Pseudomonas syringae strain, capable of colonizing the pea aphid gut, together with honeydew, enabled its transmission to the aphid offspring [33]. In the wheat aphid, nymphs cofeeding with their mother presented similar microbiomes while isolated nymphs presented much lower bacterial loads and diversity [42]. Other studies also brought evidence for plant-mediated transmission of gut-associated bacteria in aphids (Serratia symbiotica) [43] and endosymbiotic bacteria in whiteflies (Rickettsia) [44].…”

Influence of the plant interacting entomopathogenic fungus Beauveria bassiana on parasitoid host choice-behavior, development, and plant defense pathways

“…In general, wound responses, caused by chewing, induce JA-dependent genes, whereas phloem-feeding induces SA-dependent gene cascades [ 44 ]. The induction of the SA-dependent pathway by phloem-feeders overlaps that of pathogenic signatures, mainly due to the bacterial community present in these insects’ stylets, which is secreted into the plant [ 45 ]. Conversely, the JA and ET pathways overlap during plant defense responses, where the ET pathway is involved in volatile production and release to attract natural enemies, such as parasitoids [ 46 ].…”