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

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 9 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

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

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 9 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

Aphid Species Specializing on Milkweed Harbor Taxonomically Similar Bacterial Communities That Differ in Richness and Relative Abundance of Core Symbionts

Host plant range is arguably one of the most important factors shaping microbial communities associated with insect herbivores. However, it is unclear whether host plant specialization limits microbial community diversity or to what extent herbivores sharing a common host plant evolve similar microbiomes. To investigate whether variation in host plant range influences the assembly of core herbivore symbiont populations we compared bacterial diversity across three milkweed aphid species (Aphis nerii, Aphis asclepiadis, Myzocallis asclepiadis) feeding on a common host plant (Asclepias syriaca) using 16S rRNA metabarcoding. Overall, although there was significant overlap in taxa detected across all three aphid species (i.e. similar composition), some structural differences were identified within communities. Each aphid species harbored bacterial communities that varied in terms of richness and relative abundance of key symbionts. However, bacterial community diversity did not vary with degree of aphid host plant specialization. Interestingly, the narrow specialist A.asclepiadis harbored significantly higher relative abundances of the facultative symbiont Arsenophonus compared to the other two aphid species. Although many low abundance microbes were shared across all milkweed aphids, key differences in symbiotic partnerships were observed that could influence host physiology or additional ecological variation in traits that are microbially-mediated. Overall, this study suggests overlap in host plant range can select for taxonomically similar microbiomes across herbivore species, but variation in core aphid symbionts within these communities may still occur

Transcriptional responses of soybean aphids to sublethal insecticide exposure

Insecticides are a key tool in the management of many insect pests of agriculture, including soybean aphids. The selection imposed by insecticide use has often lead to the evolution of resistance by the target pest through enhanced detoxification mechanisms. We hypothesised that exposure of insecticide-susceptible aphids to sublethal doses of insecticides would result in the up-regulation of genes involved in detoxification of insecticides, revealing the genes upon which selection might act in the field. We used the soybean aphid biotype 1 reference genome, version 6.0 as a reference to analyze RNA-Seq data. We identified multiple genes with potential detoxification roles that were up-regulated 12 h after sublethal exposure to esfenvalerate or thiamethoxam. However, these genes were part of a dramatic burst of differential gene expression in which thousands of genes were up- or down-regulated, rather than a defined response to insecticides. Interestingly, the transcriptional burst observed at 12 h s declined dramatically by 24-hrs post-exposure, suggesting a general stress response that may become fine-tuned over time. Includes Supplementary Materials

Abiotic and Biotic Stressors Causing Equivalent Mortality Induce Highly Variable Transcriptional Responses in the Soybean Aphid

Environmental stress affects basic organismal functioning and can cause physiological, developmental, and reproductive impairment. However, in many nonmodel organisms, the core molecular stress response remains poorly characterized and the extent to which stress-induced transcriptional changes differ across qualitatively different stress types is largely unexplored. The current study examines the molecular stress response of the soybean aphid (Aphis glycines) using RNA sequencing and compares transcriptional responses to multiple stressors (heat, starvation, and plant defenses) at a standardized stress level (27% adult mortality). Stress-induced transcriptional changes showed remarkable variation, with starvation, heat, and plant defensive stress altering the expression of 3985, 510, and 12 genes, respectively. Molecular responses showed little overlap across all three stressors. However, a common transcriptional stress response was identified under heat and starvation, involved with up-regulation of glycogen biosynthesis and molecular chaperones and down-regulation of bacterial endosymbiont cellular and insect cuticular components. Stressor-specific responses indicated heat affected expression of heat shock proteins and cuticular components, whereas starvation altered a diverse set of genes involved in primary metabolism, oxidative reductive processes, nucleosome and histone assembly, and the regulation of DNA repair and replication. Exposure to host plant defenses elicited the weakest response, of which half of the genes were of unknown function. This study highlights the need for standardizing stress levels when comparing across stress types and provides a basis for understanding the role of general vs. stressor specific molecular responses in aphids

Abiotic and Biotic Stressors Causing Equivalent Mortality Induce Highly Variable Transcriptional Responses in the Soybean Aphid

Environmental stress affects basic organismal functioning and can cause physiological, developmental, and reproductive impairment. However, in many nonmodel organisms, the core molecular stress response remains poorly characterized and the extent to which stress-induced transcriptional changes differ across qualitatively different stress types is largely unexplored. The current study examines the molecular stress response of the soybean aphid (Aphis glycines) using RNA sequencing and compares transcriptional responses to multiple stressors (heat, starvation, and plant defenses) at a standardized stress level (27% adult mortality). Stress-induced transcriptional changes showed remarkable variation, with starvation, heat, and plant defensive stress altering the expression of 3985, 510, and 12 genes, respectively. Molecular responses showed little overlap across all three stressors. However, a common transcriptional stress response was identified under heat and starvation, involved with up-regulation of glycogen biosynthesis and molecular chaperones and down-regulation of bacterial endosymbiont cellular and insect cuticular components. Stressor-specific responses indicated heat affected expression of heat shock proteins and cuticular components, whereas starvation altered a diverse set of genes involved in primary metabolism, oxidative reductive processes, nucleosome and histone assembly, and the regulation of DNA repair and replication. Exposure to host plant defenses elicited the weakest response, of which half of the genes were of unknown function. This study highlights the need for standardizing stress levels when comparing across stress types and provides a basis for understanding the role of general vs. stressor specific molecular responses in aphids

Transcriptional responses of soybean aphids to sublethal insecticide exposure

Insecticides are a key tool in the management of many insect pests of agriculture, including soybean aphids. The selection imposed by insecticide use has often lead to the evolution of resistance by the target pest through enhanced detoxification mechanisms. We hypothesised that exposure of insecticide-susceptible aphids to sublethal doses of insecticides would result in the up-regulation of genes involved in detoxification of insecticides, revealing the genes upon which selection might act in the field. We used the soybean aphid biotype 1 reference genome, version 6.0 as a reference to analyze RNA-Seq data. We identified multiple genes with potential detoxification roles that were up-regulated 12 h after sublethal exposure to esfenvalerate or thiamethoxam. However, these genes were part of a dramatic burst of differential gene expression in which thousands of genes were up- or down-regulated, rather than a defined response to insecticides. Interestingly, the transcriptional burst observed at 12 h s declined dramatically by 24-hrs post-exposure, suggesting a general stress response that may become fine-tuned over time. Includes Supplementary Materials

Phylogenetic farming: Can evolutionary history predict crop rotation via the soil microbiome?

Agriculture has long employed phylogenetic rules whereby farmers are encouraged to rotate taxonomically unrelated plants in shared soil. Although this forms a central tenet of sustainable agriculture, strangely, this on‐farm “rule of thumb” has never been rigorously tested in a scientific framework. To experimentally evaluate the relationship between phylogenetic distance and crop performance, we used a plant–soil feedback approach whereby 35 crops and weeds varying in their relatedness to tomato (Solanum lycopersicum) were tested in a two‐year field experiment. We used community profiling of the bacteria and fungi to determine the extent to which soil microbes contribute to phenotypic differences in crop growth. Overall, tomato yield was ca. 15% lower in soil previously cultivated with tomato; yet, past the species level there was no effect of phylogenetic distance on crop performance. Soil microbial communities, on the other hand, were compositionally more similar between close plant relatives. Random forest regression predicted log10 phylogenetic distance to tomato with moderate accuracy (R2 = .52), primarily driven by bacteria in the genus Sphingobium. These data indicate that, beyond avoiding conspecifics, evolutionary history contributes little to understanding plant–soil feedbacks in agricultural fields; however, microbial legacies can be predicted by species identity and relatedness.ISSN:1752-4571ISSN:1752-456

Phylogenetic farming: Can evolutionary history predict crop rotation via the soil microbiome?

Agriculture has long employed phylogenetic rules whereby farmers are encouraged to rotate taxonomically unrelated plants in shared soil. Although this forms a central tenet of sustainable agriculture, strangely, this on‐farm “rule of thumb” has never been rigorously tested in a scientific framework. To experimentally evaluate the relationship between phylogenetic distance and crop performance, we used a plant–soil feedback approach whereby 35 crops and weeds varying in their relatedness to tomato (Solanum lycopersicum) were tested in a two‐year field experiment. We used community profiling of the bacteria and fungi to determine the extent to which soil microbes contribute to phenotypic differences in crop growth. Overall, tomato yield was ca. 15% lower in soil previously cultivated with tomato; yet, past the species level there was no effect of phylogenetic distance on crop performance. Soil microbial communities, on the other hand, were compositionally more similar between close plant relatives. Random forest regression predicted log10 phylogenetic distance to tomato with moderate accuracy (R2 = .52), primarily driven by bacteria in the genus Sphingobium. These data indicate that, beyond avoiding conspecifics, evolutionary history contributes little to understanding plant–soil feedbacks in agricultural fields; however, microbial legacies can be predicted by species identity and relatedness.ISSN:1752-4571ISSN:1752-456