Resilience of generalist predator holobionts to prey microbiome dysbiosis

Saqib, Hafiz Sohaib Ahmed

ENTOMOLOGIA GENERALIS

2026

46

4

Saqib, HSA; Chen, ZQ

Generalist predators face multiple challenges during feeding, including nutritional variability and exposure to diverse prey-associated microbes. Yet how predators prevent microbial spillovers while maintaining stable internal microbiomes remains poorly understood. This study aimed to (1) examine how dietary antibiotic-induced microbiome disruption in prey affects microbial community structure in both predator and prey, (2) characterize corresponding host transcriptomic responses across the predator-prey system, and (3) assess whether predators maintain stability through ingestion-mediated filtering, transcriptional buffering, or both. We applied an integrative multi-omics approach to the generalist predatory spider (Toxeus maxillosus) and its prey, fruit fly (Drosophila melanogaster), under controlled antibiotic treatments. Microbiome analyses revealed strong asymmetries in resilience. Prey microbiome nearly collapsed, retaining only Wolbachia, with sharp declines in alpha diversity and extensive community restructuring. This disruption coincided with pronounced transcriptomic responses, including more than 2,800 differentially expressed genes related to metabolism, immunity, and stress responses. In contrast, predators exhibited remarkable stability. Spider microbial composition and diversity remained largely unchanged despite disrupted prey microbiomes, and transcriptomic responses were modest (173 differentially expressed genes), primarily associated with lipid metabolism, proteolysis, and detoxification. Network analyses further highlight dense, positively correlated host-microbe interactions in prey, but sparse and weakly connected networks in predators, indicating functional decoupling and microbial stability. Collectively, these findings suggest that predators maintain stability through transcriptional buffering, while pre-ingestive processes associated with feeding, potentially including extra-oral digestion and venom-related bioactive compounds, may contribute to limiting the impact of dietary perturbations. This study provides an integrated microbiome-transcriptome analysis of a predator-prey system, revealing evolutionary mechanisms that may help predators maintain stability despite dietary variability.