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

  • Plant-microbe-animal interactions – original research
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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 the 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 24 h 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.

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Raw data have been made publicly available through figshare: https://doi.org/10.6084/m9.figshare.15124428.

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Acknowledgements

We thank Dr. Asher Jones for providing isolates and general input into these experiments. We appreciate Dr. W. Paul Williams for providing maize seeds. We appreciate the constructive comments by Dr. Merijn Kant and two anonymous reviewers. Funding was provided by United States Department of Agriculture NIFA Postdoctoral Fellowship 2018-67012-27979 awarded to C.J.M., US Department of Agriculture AFRI Grant 2017-67013-26596 awarded to G.W.F., and Hatch Project Grant PEN04576. This research was supported in part by the US Department of Agriculture, Agricultural Research Service. The findings and conclusions in this publication are those of the authors and should not be construed to represent any official USDA or US Government determination or policy. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US. Department of Agriculture. USDA is an equal opportunity provider and employer.

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  1. Charles J. Mason

    Present address: Tropical Crop and Commodity Protection Research Unit, Daniel K Inouye U.S. Pacific Basin Agricultural Research Center, Agricultural Research Service, USDA, 64 Nowelo Street, Hilo, HI, 96720, USA

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  1. 501 ASI Building Department of Entomology, The Pennsylvania State University, University Park, PA, 16823, USA

    Charles J. Mason, Michelle Peiffer, Abbi St Clair, Kelli Hoover & Gary W. Felton

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Contributions

CJM, KH, and GWF conceived and designed the experiments. CJM, AS, and MP performed the experiments. CJM analyzed the data. CJM, KH, and GWF wrote the manuscript and other authors provided editorial feedback.

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Correspondence to Charles J. Mason.

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Communicated by Merijn Kant.

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Mason, C.J., Peiffer, M., St Clair, A. et al. Concerted impacts of antiherbivore defenses and opportunistic Serratia pathogens on the fall armyworm (Spodoptera frugiperda). Oecologia 198, 167–178 (2022). https://doi.org/10.1007/s00442-021-05072-w

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