Population structure and gene flux of Listeria monocytogenes ST121 reveal prophages as a candidate driver of adaptation and persistence in food production environments

Abstract

Listeria monocytogenes is a bacterial pathogen found in an increasing number of food categories, potentially reflecting an expanding niche and food safety risk profile. In the UK, Listeria monocytogenes sequence type (ST) 121 is more frequently isolated from foods and food environments than from cases of clinical listeriosis, consistent with a relatively low pathogenicity. In this study, we determined the evolution associated with the environmental persistence of a Listeria monocytogenes clone by investigating clone-specific genome features in the context of the ST121 population structure from international sources. To enable unambiguous comparative genomic analysis of ST121 strains, we constructed 16 new high-quality genome assemblies from Listeria monocytogenes isolated from foods, food environments and human clinical sources in the UK from 1987 to 2019. Our dataset was supplemented with additional UK and international genomes from databases held by the Institut Pasteur and the UK Health Security Agency. Time-scaled phylogenetic reconstruction revealed that clade-specific microevolution cor-related with key characteristics that may confer adaptations important for success in the environmental niche. For example, a prophage designated LP-13-6 unique to a clade is associated with multi-year persistence in a food production setting. This prophage, observed in a strain that persisted for over a decade, may encode mechanisms facilitating environmental persis-tence, including the exclusion of other bacteriophages. Pangenome analysis provided insights into other candidate genetic elements associated with persistence and biocide tolerance. The comparative genomic dataset compiled in this study includes an international collection of 482 genome sequences that serve as a valuable resource for future studies to explore conserved genes, regulatory regions, mutations and variations associated with particular traits, such as environmental persistence, path-ogenicity or biocide tolerance.