Insect-Mediated Microbiome Engineering: A Hidden Network Shaping Plant Health and Disease Dynamics

Insects interact with plants not only as herbivores, pollinators, and seed dispersers but as persistent and often overlooked engineers of the microbial communities that colonise plant surfaces, tissues, vascular systems, and roots. Every time an insect feeds on a plant, visits a flower, lays eggs in plant tissue, or tunnels through bark, it performs a microbial act, depositing salivary microorganisms, creating wound portals through which environmental microbes can enter, and triggering hormonal changes in the plant that reshape the chemical environment available to resident and incoming microbial communities. Beyond feeding, insects carry specialised microbial associates, fungi, bacteria, phytoplasmas, and spiroplasmas, whose dispersal and establishment in plant hosts depends entirely on insect activity. Bark beetles introduce wood-rotting and vessel-blocking fungi with lethal efficiency into tree vascular systems; sharpshooter leafhoppers deposit vascular-colonising bacteria into the xylem of perennial crops; pollinators shuttle yeasts and bacteria between flowers, seeding floral microbiomes that influence plant reproductive success and pathogen susceptibility. These are not incidental microbial transfers, in many cases they are fundamental to the ecology of both the insect and the plant. Yet the systematic study of insects as agents of plant microbiome engineering, and the consequences of that engineering for plant health and disease, remains fragmented across entomology, plant pathology, microbial ecology, and plant biology in ways that have slowed both mechanistic understanding and applied translation.The mechanisms through which insects restructure plant-associated microbiomes operate simultaneously at multiple scales. At the point of feeding or oviposition, insect saliva introduces a microbiome that is specific to the insect species, colony, and nutritional state, and that can include both pathogenic and mutualistic organisms capable of persisting and proliferating in plant tissue. Wound surfaces created by chewing, piercing-sucking, or boring provide a microbially accessible interface that would otherwise be sealed by the plant cuticle or bark; the succession of microorganisms colonising these sites shapes the trajectory of healing, susceptibility to secondary infection, and in some cases the systemic defensive state of the whole plant. Herbivory-induced changes to plant hormone signalling, particularly the rapid activation of the jasmonate pathway and its complex antagonistic interactions with salicylate, alter the chemical composition of root exudates, leaf surface secretions, and phloem chemistry in ways that are increasingly recognised as powerful modulators of plant-associated microbiome structure across all compartments. Gall-forming insects produce perhaps the most dramatic example of this engineering: they induce the formation of entirely novel plant organs with distinct microenvironments, metabolite profiles, and microbial communities that diverge profoundly from surrounding tissue. More subtly, the sustained presence of phloem-feeding insects alters rhizosphere microbiome composition in ways detectable well below ground from above-ground feeding sites, reflecting the systemic metabolic integration of the plant and its capacity to relay above-ground stress signals to below-ground microbial communities. The net effect of all these processes is that the plant microbiome encountered in a real agricultural setting is not simply the product of soil, air, and dispersal, it is actively and continuously shaped by the insect community sharing the plant’s environment.Despite the ecological importance of these dynamics, insect-mediated microbiome engineering remains under characterised and under integrated as a research field. Studies linking herbivory or pollinator activity to shifts in plant microbiome composition are accumulating, but the mechanistic connections between specific insect activities, the microbiome changes they trigger, and the downstream consequences for plant health and disease resistance are rarely followed through comprehensively. The role of insect frass as a microbial inoculant, delivering viable and sometimes virulent microorganisms directly to plant surfaces and surrounding soil, has received limited systematic attention. The temporal dynamics of microbiome recovery following the cessation of insect pressure, and whether persistent insect-mediated microbiome shifts alter susceptibility during subsequent pathogen challenge, remain largely unexplored. And the possibility of deliberately exploiting insect behaviour to deliver beneficial microorganisms to plant tissues, using insects as living microbial dispersal agents for biocontrol or microbiome restoration, represents an emerging biotechnological frontier that sits squarely at the intersection of entomology, microbiology, and crop science. This Research Topic aims to consolidate and advance the field by bringing together researchers across these disciplines to map the scope of insect-mediated microbiome engineering, characterise its underlying mechanisms, and evaluate its significance for plant health and disease in both natural and managed systems.We welcome Original Research, Review, Mini Review, Methods, Hypothesis and Theory, Perspective, and Opinion articles addressing, but not limited to, the following themes:• Insect saliva-associated microbiomes and their transfer to plant tissues during feeding: composition, host specificity, persistence within plant compartments, and effects on local and systemic plant microbiome structure• Wound microbiome dynamics following insect herbivory: microbial succession at feeding and oviposition sites, competition between introduced and resident microorganisms, and consequences for plant healing and secondary infection susceptibility• Herbivory-induced plant hormone signalling, jasmonate, salicylate, ethylene, and abscisic acid, and downstream effects on root exudate chemistry, leaf metabolite profiles, and plant-associated microbiome composition across above- and below-ground compartments• Insect vectors of bacterial, fungal, oomycete, and phytoplasmal plant pathogens: transmission mechanisms, establishment dynamics within plant vascular and mesophyll tissues, and epidemiological consequences at field and landscape scales• Bark beetle and wood-boring insect symbioses with fungi and bacteria: mechanisms of microbial introduction and establishment, plant vascular defence responses, and the contribution of microbiome disruption to tree mortality and forest decline• Gall-forming insects as microbiome engineers: the structure and function of gall-associated microbial communities, their metabolic interactions with the host plant, and their consequences for host physiology and susceptibility to other pathogens• Systemic effects of above-ground herbivory on below-ground microbiome composition: root exudate shifts, rhizosphere community restructuring, and implications for soil-borne pathogen and beneficial microbe dynamics• Pollinator-mediated microbiome transfer: the role of bees and other floral visitors in dispersing bacteria, fungi, and yeasts between flowers, and consequences for floral microbiome composition, plant reproductive biology, and pathogen transmission in flowering crops• Insect frass as a microbial inoculant: community composition, viability of delivered microorganisms, and measurable effects on plant surface, endophytic, and soil microbial communities• Temporal dynamics of plant microbiome recovery following insect pressure, the persistence of insect-mediated community shifts, and their role in altering subsequent plant susceptibility to pathogens and abiotic stress• Insect community diversity, pest management practices, and insecticide use as determinants of plant microbiome composition at field and landscape scales• Deliberate exploitation of insect behaviour for beneficial microorganism delivery: insects as vectors for biocontrol agents, probiotic microbes, and microbiome restoration strategies in managed agricultural systems• Multi-omics approaches, including metagenomics, metatranscriptomics, metabolomics, and volatilomics , applied to characterising the dynamics of insect-mediated microbiome engineering across plant compartments and timescales Topic editors: Mubasher Hussain, Mehraj D. Shah Source: https://www.frontiersin.org/research-topics/82522/insect-mediated-microbiome-engineering-a-hidden-network-shaping-plant-health-and-disease-dynamics