Lineage-specific evolution and gene flow in Listeria monocytogenes are independent of bacteriophages.

Roxana Zamudio,Roger Stephan,Richard D Haigh,Taurai Tasara,Megan De Ste Croix,Andrew D Millard,Stephen D Bentley,Marco R Oggioni,Katrin Zurfluh,Joseph D Ralph,Min Jung Kwun,Nicholas J Croucher

doi:10.1111/1462-2920.15111

Abstract

Listeria monocytogenes is a foodborne pathogen causing systemic infection with high mortality. To allow efficient tracking of outbreaks a clear definition of the genomic signature of a cluster of related isolates is required, but lineage-specific characteristics call for a more detailed understanding of evolution. In our work, we used core genome MLST (cgMLST) to identify new outbreaks combined to core genome SNP analysis to characterize the population structure and gene flow between lineages. Whilst analysing differences between the four lineages of L. monocytogenes we have detected differences in the recombination rate, and interestingly also divergence in the SNP differences between sub-lineages. In addition, the exchange of core genome variation between the lineages exhibited a distinct pattern, with lineage III being the best donor for horizontal gene transfer. Whilst attempting to link bacteriophage-mediated transduction to observed gene transfer, we found an inverse correlation between phage presence in a lineage and the extent of recombination. Irrespective of the profound differences in recombination rates observed between sub-lineages and lineages, we found that the previously proposed cut-off of 10 allelic differences in cgMLST can be still considered valid for the definition of a foodborne outbreak cluster of L. monocytogenes.

Highlights

Listeria monocytogenes, one of the most important foodborne pathogens, is the causative agent of Listeriosis, an infection that affects the elderly, immuno-compromised individuals, and pregnant women (Radoshevich and Cossart, 2017; Lamond and Freitag, 2018)
Irrespective of the profound differences in recombination rates observed between sub-lineages and lineages, we found that the previously proposed cut-off of 10 allelic differences in core genome MLST (cgMLST) can be still considered valid for the definition of a foodborne outbreak cluster of L. monocytogenes
With the advent of low-cost whole-genome sequencing in the past few years, outbreak analysis has shifted from the previous gold standard of PFGE analysis to core genome multilocus sequencing (Lüth et al, 2018). cgMLST is based upon just the genes present in the core genome of a species, or at least those present in the panel of genomes available for analysis (Ruppitsch et al, 2015)

Summary

Introduction

One of the most important foodborne pathogens, is the causative agent of Listeriosis, an infection that affects the elderly, immuno-compromised individuals, and pregnant women (Radoshevich and Cossart, 2017; Lamond and Freitag, 2018). A number of large listeriosis outbreaks have been seen worldwide, including the latest one reported in 2017–2018 in South Africa, which was caused by the consumption of contaminated ready-to-eat processed meat products from one company (WHO, 2018; Smith et al, 2019). This means that surveillance of outbreaks is a major concern for national and international authorities. More recently after analysis of isolates with a known epidemiological link, it was proposed that this cut-off value should be reduced to ≤7 cgMLST allele differences (Moura et al, 2016)

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Conclusion