Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

Abstract

Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host‐plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival × reproduction) by 74 ± 10% and 92 ± 2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host‐plant defenses a 1.4‐fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1‐stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5‐fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3‐fold) and Wolbachia increasing (1.5‐fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi‐locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host‐symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.

Developmental and Ecological Benefits of the Maternally Transmitted Microbiota in a Dung Beetle

“…The ability of obligate and facultative microbial symbionts to shape the desiccation or thermal tolerance of their hosts has been documented in multiple animal and plant species (Gilbert et al 2010;Rolli et al 2015). For instance, the thermal environment of hosts can strongly shape both the composition and gene expression of their associated microbial communities (Thurber et al 2009;Lokmer and Wegner 2015;Enders and Miller 2016), and stressful temperature conditions have been shown to favor the retention and proliferation of symbionts that confer heat tolerance to hosts in natural populations (e.g., Montllor et al 2002;Berkelmans and van Oppen 2006). While the mechanisms underlying increased thermotolerance are poorly understood, an increasing number of studies suggest that symbionts may contribute to host thermotolerance by inducing the expression of host heat shock or cytoskeletal proteins that contribute to heat tolerance (Dunbar et al 2007;McLellan et al 2007;Brumin et al 2011).…”

Effects of different temperature regimes on survival of Diaphorina citri and its endosymbiotic bacterial communities

“…In the aphid, the resistance to its associated parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) involved Candidatus Hamiltonella defensa, but this effect reduced under heat stress (Bensadia et al, 2006). In spite of that, aphid clones infected with Candidatus Hamiltonella defensa remain highly resistant to A. ervi under heat shock (Bensadia et al, 2006;Guay et al, 2009;Enders and Miller, 2016). Besides, the obligate endosymbionts may also have an effect on aphid (Barribeau et al, 2010;Burke et al, 2010).…”

Differences in Microbiota Between Two Multilocus Lineages of the Sugarcane Aphid (Melanaphis sacchari) in the Continental United States

“…and Serratia spp. are reported to have biologically relevant functions at low abundances in other aphids (Enders and Miller 2016). Interestingly, Rickettsiella, which is known to alter body color in pea aphids (Tsuchida et al 2010), was found in SCA and if similar in function, might influence the attractiveness of SCA to natural enemies (i.e., predators and parasitoids).…”