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Oregano essential oil reduces the virulence of Vibrio parahaemolyticus causing acute hepatopancreatic necrosis disease (AHPND) in Penaeus vannamei

Abstract:

Acute Hepatopancreatic Necrosis Disease (AHPND), caused by several Vibrio species, results in high mortality rates in penaeid shrimp aquaculture worldwide. Plant-derived essential oils have shown promising potential for controlling vibriosis in shrimp culture. Thus, we investigated the antivirulence effects of oregano essential oil (OEO) at sub-minimum inhibitory concentrations (sub-MIC) on four virulence phenotypes (exopolysaccharide, biofilm, swimming motility and swarming motility) in Vibrio parahaemolyticus, the causative agent of AHPND. The antivirulence effect of OEO was validated through a challenge test by infecting Penaeus vannamei shrimp with V. parahaemolyticus cultured with or without OEO. Additionally, transcriptomic analysis was performed to compare the transcriptional regulation of V. parahaemolyticus with and without OEO addition to identify therapeutic targets at the molecular level. All four virulence phenotypes were significantly inhibited (p < 0.05) in a concentration-dependent manner. Upon in vivo challenge, the mortality of V. parahaemolyticus-infected shrimp (56 ± 5%) cultured with OEO was significantly (p < 0.05) lower than that of the control group (93 ± 5%). Transcriptomic analysis revealed 89 downregulated differentially expressed genes (DEGs) associated with membrane integrity, ribosomes, motility, transport, type VI secretion system (T6SS), and enzymes involved in energy metabolism, and 94 upregulated DEGs linked to biosynthetic processes, regulatory proteins, osmoadaptation, and other molecular processes. Consistent with the transcriptomic results, RT-qPCR analysis showed that genes encoding lafA, ompW, pirA, and pirB were significantly downregulated at 1 μg mL<sup>-1</sup>. These findings suggest that OEO acts via multiple therapeutic pathways, inhibiting V. parahaemolyticus virulence. Our study demonstrated the significant antivirulence effect of OEO on V. parahaemolyticus, highlighting its potential as a viable and environmentally friendly alternative to traditional antibiotics for controlling AHPND in shrimp aquaculture.