Gut interkingdom predator-prey interactions are key determinants of shrimp health

Abstract Intensive studies have focused on external factors governing the gut microbiota-disease relationship. It remains unknown how internal gut microbial components, especially interkingdom predators — phagotrophs and Bdellovibrio and like organisms (BALOs) — are linked to host health. Herein, we integrated the holistic gut microbiome including pathogens, bacteria, protists, predators, functional pathways, and shrimp immune potentials, to identify the gut microbial components that were indicative of shrimp white feces syndrome (WFS) onset. Both diversities and structures of the gut BALOs and phagotrophs communities differed significantly at the WFS onset stage, but not of the gut bacterial and protistan counterparts. Pathogens dynamics were best predicted by the gut BALOs or phagotrophs. Notably, nine WFS discriminatory phagotrophic taxa contributed 78.6% diagnose accuracy of shrimp health status at the WFS onset stage. The differential functional pathways were intimately associated with BALOs. There were intensive interactions among pathogens, gut BALOs, phagotrophs, and shrimp immune potentials. Specifically, shrimp activate multiple signaling pathways in response to WFS. However, pathogens encode virulence factors that neutralize and evade shrimp immune clearance, thereby leading to WFS outbreak. Collectively, we proposed a conceptual model to infer the etiology of shrimp WFS. Our findings bridge the interplay among interkingdom predator-prey interactions, pathogens invasion, host immune feedbacks, and disease progression, which greatly broaden our understanding of shrimp WFS etiology from ecological and molecular perspectives.