The role and the determination of the LuxI protein binding targets in the formation of biogenic amines in Hafnia alvei H4

Abstract

Hafnia alvei is a spoilage microorganism that possesses the LuxI/LuxR-type quorum sensing (QS) system. Biogenic amines (BAs) are important in food spoilage and safety, yet the role of QS in BA formation remains poorly understood. This study investigated the ability of H. alvei H4 to produce BAs in fish flesh and decarboxylase culture media. The findings showed that H. alvei H4 produced substantial amounts of putrescine and cadaverine in turbot flesh, with its enhanced amine-producing capacity potentially leading to the eventual deterioration of the fish. Furthermore, the deletion of the QS element—AHL synthase gene luxI—affected the concentrations of both BAs. Based on these observations, the present study conducted multifaceted experiments, including phenotypic assessments and analyses of gene expression, to explore the role of luxI and to identify its specific binding targets. The results indicated that putrescine formation in H. alvei H4 primarily occurred via the arginine deiminase (ADI) pathway, with luxI playing a positive role in the conversion of arginine to ornithine and subsequently to putrescine. The reduction in putrescine content observed in a luxI mutant (ΔluxI) was attributed to the direct binding of the LuxI protein to the promoters of the argF and speC genes, which code for ornithine carbamoyltransferase and ornithine decarboxylase, respectively. The findings of this study provided the basis to understand the influence of QS on BA production in H. alvei, by specifically demonstrating the involvement of the luxI gene on putrescine and cadaverine production.