Abstract
BackgroundWhile increasing data on bacterial evolution in controlled environments are available, our understanding of bacterial genome evolution in natural environments is limited. We thus performed full genome analyses on four Listeria monocytogenes, including human and food isolates from both a 1988 case of sporadic listeriosis and a 2000 listeriosis outbreak, which had been linked to contaminated food from a single processing facility. All four isolates had been shown to have identical subtypes, suggesting that a specific L. monocytogenes strain persisted in this processing plant over at least 12 years. While a genome sequence for the 1988 food isolate has been reported, we sequenced the genomes of the 1988 human isolate as well as a human and a food isolate from the 2000 outbreak to allow for comparative genome analyses.ResultsThe two L. monocytogenes isolates from 1988 and the two isolates from 2000 had highly similar genome backbone sequences with very few single nucleotide (nt) polymorphisms (1 – 8 SNPs/isolate; confirmed by re-sequencing). While no genome rearrangements were identified in the backbone genome of the four isolates, a 42 kb prophage inserted in the chromosomal comK gene showed evidence for major genome rearrangements. The human-food isolate pair from each 1988 and 2000 had identical prophage sequence; however, there were significant differences in the prophage sequences between the 1988 and 2000 isolates. Diversification of this prophage appears to have been caused by multiple homologous recombination events or possibly prophage replacement. In addition, only the 2000 human isolate contained a plasmid, suggesting plasmid loss or acquisition events. Surprisingly, besides the polymorphisms found in the comK prophage, a single SNP in the tRNA Thr-4 prophage represents the only SNP that differentiates the 1988 isolates from the 2000 isolates.ConclusionOur data support the hypothesis that the 2000 human listeriosis outbreak was caused by a L. monocytogenes strain that persisted in a food processing facility over 12 years and show that genome sequencing is a valuable and feasible tool for retrospective epidemiological analyses. Short-term evolution of L. monocytogenes in non-controlled environments appears to involve limited diversification beyond plasmid gain or loss and prophage diversification, highlighting the importance of phages in bacterial evolution.
Highlights
While increasing data on bacterial evolution in controlled environments are available, our understanding of bacterial genome evolution in natural environments is limited
Determination of genome sequences for three L. monocytogenes isolates obtained from foods and human listeriosis cases linked to a single food processing facility, in conjunction with a previously reported genome sequence for a food isolate linked to the same facility [28], provided a unique resource to gain insight into the short-term evolution of L. monocytogenes in non-controlled environments
Short term evolution of L. monocytogenes in natural environments can involve considerable phage mediated diversification and loss or gain of plasmids While a few singletons were observed in the genome backbone of the two 1988 and the two 2000 isolates, the only polymorphisms that differentiate the 1988 isolates from the 2000 isolates fall within the two prophages inserted into comK and tRNA-Thr-4
Summary
While increasing data on bacterial evolution in controlled environments are available, our understanding of bacterial genome evolution in natural environments is limited. We performed full genome analyses on four Listeria monocytogenes, including human and food isolates from both a 1988 case of sporadic listeriosis and a 2000 listeriosis outbreak, which had been linked to contaminated food from a single processing facility. Evolved lineages of bacteria have provided important data on mechanisms involved in short-term bacterial evolution and adaptation [1,2,3] in simple controlled environments. Important differences between experimental and natural bacterial populations include (i) population sizes that are much greater in experimental populations than in a natural population; (ii) generation times that are probably much shorter in an experimental population than in a natural population; and (iii) absence of donors of genetic materials, which allow for rapid diversification via horizontal gene transfer (e.g., other bacteria, bacteriophages). 12 Escherichia coli populations that originated from the same parent strain all showed substitutions in the same candidate genes after they were cultured for 20,000 generations under identical conditions [5]
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