Prevalence and stable acquisition of biogenic amine-synthesizing genes in lactic acid bacteria across diverse niches: implications for food safety and human health

Biogenic amines (BAs) are metabolites produced by lactic acid bacteria (LAB) with implications for food safety and human health. Despite extensive phenotypic studies on individual BA biosynthesis genes, the distribution, evolutionary dynamics, ecological associations, and mobility mechanisms underpinning BA biosynthesis across LAB strains is unclear. Here, we conducted the first comprehensive genomic survey of 4880 LAB genomes to elucidate the prevalence and mobility of key BA genes. Ornithine decarboxylase (odc) showed a broader taxonomic distribution, while tyrosine decarboxylase (tdc), although predominant, was confined to Enterococcus. All BA genes exhibited strong ecological associations, suggesting niche-specific adaptation. Phylogenomic analysis highlighted complex evolutionary trajectories involving ancestral gains and extensive horizontal gene transfer (HGT), particularly for odc and tdc genes. Gene synteny and compositional signatures further supported lineage-specific retention and recurrent HGT events among phylogenetically related taxa. For example, the arginine decarboxylase (adc) gene and agmatinase were potentially co-acquired as an operon-level unit. Codon usage suggested translational assimilation, reflecting the functional integration of BA genes in LAB. Insertion sequences and composite transposons were predicted as putative vectors mediating BA gene mobility. Collectively, this study provides a framework linking BA gene distribution to niche and mobility, with implications for risk assessment in foods and probiotics.