Concerted impacts of antiherbivore defenses and opportunistic Serratia pathogens on the fall armyworm (Spodoptera frugiperda)

Authors: Mason, Charles; PEIFFER, MICHELLE - Pennsylvania State University; ST CLAIR, ABBI - Pennsylvania State University; HOOVER, KELLI - Pennsylvania State University; FELTON, GARY - Pennsylvania State University

Submitted to: Oecologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2021
Publication Date: 11/6/2021
Citation: Mason, C.J., Peiffer, M., St Clair, A., Hoover, K., Felton, G.W. 2021. Concerted impacts of antiherbivore defenses and opportunistic Serratia pathogens on the fall armyworm (Spodoptera frugiperda). Oecologia. 198:167-178. https://doi.org/10.1007/s00442-021-05072-w.
DOI: https://doi.org/10.1007/s00442-021-05072-w

Interpretive Summary: Insects are in constant contact with microbiota. Some of microbes cause no ill effects, but can become pathogenic when the insect is compromised by environmental stressors. Herbivores often encounter plants exhibiting different levels of resistance, which may trigger the switch of a microbe from being benign to pathogenic. In the present study, we determined how the larval fall armyworm interacted with Serratia initially isolated from healthy caterpillars. We evaluate the pathogenicity of these strains through different circumstances, including how they performed on different diets. Injection bioassays revealed that the Serratia isolates differed levels of pathogenicity, with some strains having no effects while others causing rapid mortality. Diets mediated mortality of the highly pathogenic strains. Larvae had low levels (<7%) of mortality on artificial, but had high levels of mortality on the different plants. Mortality from Serratia feeding on maize exceeded 50% on one genotype and 90% on another. Tomato and soybean further indicated elevated mortality due to Serratia compared to artificial diets and differences between plant genotypes. Our results indicate plants can facilitate the initial stress that generates pathogenic interactions in Serratia. The ability of resident gut bacteria to switch from a commensal to pathogenic lifestyle has significant ramifications for the host and is likely a broader phenomenon in multitrophic interactions facilitated by plant defenses. Results from this research provides better knowledge of how microbes and plants may be leveraged for managing insect populations.

Technical Abstract: Insects frequently confront different microbial assemblages. Bacteria inhabiting an insect gut are often commensal, but some can become pathogenic when the insect is compromised from different stressors. Herbivores are often confronted by various forms of plant resistance, but how defenses generate opportunistic microbial infections from residents in the gut are not well understood. In this study, we evaluated pathogenic tendencies of Serratia isolated from the digestive system of healthy fall armyworm larvae (Spodoptera frugiperda) and how it interfaces with plant defenses. We initially selected Serratia strains that varied in their direct expression of virulence factors. Inoculation of the different isolates into the fall armyworm body cavity indicated differing levels of pathogenicity, with some strains exhibiting no effects while others causing mortality 24h after injection. Oral inoculations of pathogens on larvae provided artificial diets caused marginal (<7%) mortality. However, when insects were provided different maize genotypes, mortality from Serratia increased and was higher on plants exhibiting elevated levels of herbivore resistance (<50% mortality). Maize defenses facilitated an initial invasion of pathogenic Serratia into the larval hemocoel¸ which was capable of overcoming insect antimicrobial defenses. Tomato and soybean further indicated elevated mortality due to Serratia compared to artificial diets and differences between plant genotypes. Our results indicate plants can facilitate the incipient emergence of pathobionts within gut of fall armyworm. The ability of resident gut bacteria to switch from a commensal to pathogenic lifestyle has significant ramifications for the host and is likely a broader phenomenon in multitrophic interactions facilitated by plant defenses.