Integrating bacteriophage-mediated gene mobility into microbiological risk assessment: A framework for food safety

Bacteriophages occupy a structurally contradictory position in modern food systems. Since 2006 they have been approved in multiple jurisdictions as biocontrol agents applied directly to food, and are now routinely deployed against Listeria monocytogenes, Escherichia coli O157:H7 and Salmonella enterica. In parallel, phages are the principal vehicles of transduction, the horizontal transfer mechanism by which antimicrobial resistance genes (ARGs) and virulence determinants move between bacterial cells. Current microbiological risk assessment (MRA) frameworks resolve this asymmetrically: phage biocontrol enters quantitative models as a log-reduction term, whereas phage-mediated gene mobility is rarely represented explicitly. Current evidence suggests that this pathway now warrants explicit consideration. The discovery of lateral transduction, which mobilises chromosomal regions at frequencies orders of magnitude above classical generalised transduction, indicates that phage-mediated transfer is, in the systems where it has been measured, not a rare packaging error but a routine feature of temperate phage life cycles, although its prevalence, rates, host range and ecological importance across food-associated communities remain insufficiently resolved. Concurrently, viromics, whole-genome sequencing, proximity ligation and emerging transductomic approaches have made the food-chain phageome quantifiable for the first time. Here we argue that, to our knowledge, the phageome constitutes a largely unaddressed blind spot in microbiological risk assessment, and we set out a framework for closing it. We map phage-mediated gene mobility onto the four Codex risk-analysis steps, identify the specific omics measurements that would populate each step and specify the model structures required to propagate transduction through exposure and risk characterisation. We also propose genomic screening criteria for phage biocontrol products proportionate to their transducing capacity. We conclude that phage-aware risk assessment is now technically tractable and that the principal obstacles are the absence of standardised quantification protocols, the scarcity of transduction-frequency data in real food matrices, and the lack of model structures capable of representing gene flow rather than organism flow.