Cellular Immune Responses and Gut Microbiome Diversity of Adult Tomato Leaf Miner (Phthorimaea absoluta) when Exposed to Entomopathogenic Fungal Isolates

Abstract

The tomato leaf miner, Phthorimaea absoluta, is a highly destructive pest of tomatoes and other solanaceous crops. Chemical insecticides remain the primary strategy used to control this pest. However, the growing threat of insecticide resistance prompts the urgent need to develop alternative, sustainable, and eco-friendly pest control approaches. Entomopathogenic fungi (EPF) present a potential alternative to chemical insecticides due to their ability to overcome insecticide resistance and negligible effect on non-target organisms. However, most studies investigating host-pathogen interactions have mainly focused on evolutionary and functional aspects, leaving a knowledge gap about the physiological mechanisms underlying the efficacy of EPF as biocontrol agents. In this randomized controlled study, newly emerged P. absoluta moths were exposed to three isolates of M. anisopliae (ICIPE 665, ICIPE 20, and ICIPE 18) for three minutes in a contamination device. The fungus-challenged P. absoluta adults and their control counterparts were incubated at, 15°C, 20°C, 25°C, and 30°C, for 10 days and were studied for survival, cellular immune responses, and gut microbiome diversity shifts. Findings from this study showed that at 25°C -the optimum temperature for M. anisopliae, the survival rate of challenged P. absoluta moths was remarkably low, less than 50%, with ICIPE 18 causing the highest (80%) mortality rate. At the same time, ICIPE 20 triggered the highest significant decline in total hemocyte counts (THCs) in the host insects at 25ºC, 10 days post-infection (p <0.001). Additionally, ICIPE 18 and ICIPE 20 induced significant shifts in the microbiota of P. absoluta, increasing the relative abundance of Wolbachia, -the dominant microbe, by 20.94% and 27.68%, respectively, at 25ºC, 10 days post-exposure. These results demonstrate that cellular immune responses are central to pathogen-pest interaction and further suggest that ICIPE 18 and ICIPE 20 present greater potential as biocontrol agents of P. absoluta in solanaceous cropping systems.