Pathobiology of Enterocytozoon hepatopenaei (EHP) in shrimp: Diagnosis and interpretation from the gut bacterial community

Abstract

It is now widely recognized that the gut microbiota contributes indispensible roles in improving host health and fitness. Thus, dysbiosis in the gut microbiota frequently causes host disease, and vise versa. However, it remains unclear how interkingdom infection, such as eukaryotic Enterocytozoon hepatopenaei (EHP), affects the host gut bacterial community. To address this pressing knowledge, we explored how the shrimp gut bacterial community, digestive and immune activities responded to EHP infection. Result showed that the measured digestion activities in EHP infected shrimp were significantly lower than these in healthy subjects, while immune activities exhibited the opposite trend. A structural equation modeling (SEM) revealed that EHP infection directly altered the gut bacterial community and enzyme activities, which further affected the growth traits of shrimp. In particular, we identified 20 EHP infection discriminatory-taxa that accurately distinguished (100% accuracy) healthy shrimp from EHP infected individuals. EHP infection caused more dispersion, lower modularity, decreased proportion of negative correlations and keystone taxa of the gut microbiota, thereby leading to an unstable gut microbiota. Going forward, EHP infected shrimp are prone to be suffered by bacterial pathogens, as supported by compromised immune system and enhanced bacterial infection disease pathways. Collectively, eukaryotic EHP infection compromises shrimp energy metabolisms and the stability of gut microbiota, which in turn increase the susceptibility of pathogens colonization (e.g., enriched abundances of potential pathogens) and retard the growth of EHP infected shrimp. These findings provide novel insights into the pathobiology of parasitic EHP from both biology and ecological perspectives.