Microbial Symbiosis in Lepidoptera: Analyzing the Gut Microbiota for Sustainable Pest Management

Abstract

Recent advances in microbiome studies have deepened our understanding of endosymbionts and gut-associated microbiota in host biology. Of those, lepidopteran systems in particular harbor a complex and diverse microbiome with various microbial taxa that are stable and transmitted between larval and adult stages, and others that are transient and context-dependent. We highlight key microorganisms-including Bacillus, Lactobacillus, Escherichia coli, Pseudomonas, Rhizobium, Fusarium, Aspergillus, Saccharomyces, Bifidobacterium, and Wolbachia-that play critical roles in microbial ecology, biotechnology, and microbiome studies. The fitness implications of these microbial communities can be variable; some microbes improve host performance, while others neither positively nor negatively impact host fitness, or their impact is undetectable. This review examines the central position played by the gut microbiota in interactions of insects with plants, highlighting the functions of the microbiota in the manipulation of the behavior of herbivorous pests, modulating plant physiology, and regulating higher trophic levels in natural food webs. It also bridges microbiome ecology and applied pest management, emphasizing S. frugiperda as a model for symbiont-based intervention. As gut microbiota are central to the life history of herbivorous pests, we consider how these interactions can be exploited to drive the development of new, environmentally sound biocontrol strategies. Novel biotechnological strategies, including symbiont-based RNA interference (RNAi) and paratransgenesis, represent promising but still immature technologies with major obstacles to overcome in their practical application. However, microbiota-mediated pest control is an attractive strategy to move towards sustainable agriculture. Significantly, the gut microbiota of S. frugiperda is essential for S. frugiperda to adapt to a wide spectrum of host plants and different ecological niches. Studies have revealed that the microbiome of S. frugiperda has a close positive relationship with the fitness and susceptibility to entomopathogenic fungi; therefore, targeting the S. frugiperda microbiome may have good potential for innovative biocontrol strategies in the future.

Keywords: endosymbionts; gut microbiota; insect–plant interactions; microbiome pest management.

Figure 1

Schematic illustration of the gut microbiota of lepidopteran insects. The figure depicts the different microbe communities: intracellular endosymbionts and extracellular ectosymbionts of an insect gut. It portrays the relationship of these microbes with the host, and focuses on functions, such as nutrient provisioning, digestion, detoxification, and insect behavior modulation. The diagram also indicates the dynamics of microbial transmission, the impact of environmental and dietary conditions on microbiota, and the putative functions of these microbes in insect–plant interactions.

Figure 2

Host phylogeny COI-based and gut microbial abundance across insect–plant system (A,B). Maximum-likelihood phylogeny of insect hosts with radar plot shows microbial taxon abundance (C). The blue-colored line indicates mean, and the red-colored line denotes standard deviation (Sd) of the co-abundance profile of the microbiome in the gut of lepidopterans.

Figure 3

Functional diversity of the Lepidoptera microbiome. Multifaceted strategies employed by Fall Armyworm (S. frugiperda) to thrive in its environment, including defense mechanisms, metabolic adaptations, and ecological interactions.

Figure 4

Roles of gut bacteria in influencing insect behavior and physiology. Gut bacteria mediate plant selection preferences in insects, aiding in the identification of suitable host plants. Gut bacteria help insects overcome feeding challenges such as low nutrient availability, indigestible plant tissues, and plant toxins. Dysbiosis in the gut microbiota caused by plant defenses or inadequate nutrition can be detrimental or lethal to insects.

Figure 5

Gut microbiota impact plant–insect associations and third trophic-level organisms through either synergistic or antagonistic interactions with pathogens, and by the exhalation of volatile organic compounds (VOCs) that can attract or repel natural enemies. These mechanisms showcase the diversity of ecological roles of gut bacteria in insect-mediated interactions.

Figure 6

Gut microbiotas hold significant potential as pest management agents by influencing the biology of insect gut bacteria in insect–plant interactions. They modulate pathogens by either enhancing or inhibiting pest control agents and interact with natural enemies of host pests through the release of volatile organic compounds (VOCs). This figure depicts how gut microbiotas impact pest dynamics, influencing plant–pest relationships, pathogen control, and interactions with natural predators, ultimately contributing to sustainable pest management strategies.