Interplay of vertical inheritance and horizontal gene transfer shapes biogenic amine biosynthesis in lactic acid bacteria: Implications for food safety

Introduction

Biogenic amines (BAs) produced by lactic acid bacteria (LAB) are important determinants of food quality and safety due to their potential adverse effects on human health. While the BA production in LAB has been extensively reported, the evolutionary mechanisms responsible for the origin, maintenance, and dissemination of BA biosynthesis genes remain poorly understood. This study aimed to elucidate the relative contributions of vertical inheritance and horizontal gene transfer (HGT) to the evolution of BA-producing traits in LAB.

Methods

A comparative genomic analysis was performed on 4,880 publicly available LAB genomes. Key BA biosynthesis genes, including ornithine decarboxylase (odc), tyrosine decarboxylase (tdc), histidine decarboxylase (hdc), arginine decarboxylase (adc), and agmatinase, were identified and analyzed. Phylogenomic reconstruction, ancestral state reconstruction, gene synteny analysis, nucleotide composition profiling, codon usage analysis, and mobile genetic element screening were employed to investigate gene evolutionary histories and mechanisms of acquisition.

Results

BA biosynthesis genes followed diverse evolutionary trajectories involving ancestral gains and extensive HGT, particularly for odc and tdc genes across LAB lineages. Phylogenetic incongruence, conserved syntenic arrangements, and compositional analyses supported multiple independent acquisition events. The adc and agmatinase genes frequently occurred as a conserved genetic unit, suggesting coordinated acquisition and maintenance. Codon usage patterns indicated translational adaptation following gene acquisition, while insertion sequences and composite transposons were commonly associated with BA loci, highlighting their potential role in gene mobilization.

Conclusions

The evolution of BA biosynthesis genes in LAB is driven by a dynamic interplay between vertical inheritance and HGT. Stable retention following acquisition and the involvement of mobile genetic elements have facilitated the persistence of BA-producing traits across LAB lineages. These findings offer novel insights into the evolutionary mechanisms underlying BA production and support genomic approaches for improving the safety assessment of food-associated and probiotic LAB strains.