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A new perspective on Listeria monocytogenes evolution.

ABSTRACT: Listeria monocytogenes is a model organism for cellular microbiology and host-pathogen interaction studies and an important food-borne pathogen widespread in the environment, thus representing an attractive model to study the evolution of virulence. The phylogenetic structure of L. monocytogenes was determined by sequencing internal portions of seven housekeeping genes (3,288 nucleotides) in 360 representative isolates. Fifty-eight of the 126 disclosed sequence types were grouped into seven well-demarcated clonal complexes (clones) that comprised almost 75% of clinical isolates. Each clone had a unique or dominant serotype (4b for clones 1, 2 and 4, 1/2b for clones 3 and 5, 1/2a for clone 7, and 1/2c for clone 9), with no association of clones with clinical forms of human listeriosis. Homologous recombination was extremely limited (r/m<1 for nucleotides), implying long-term genetic stability of multilocus genotypes over time. Bayesian analysis based on 438 SNPs recovered the three previously defined lineages, plus one unclassified isolate of mixed ancestry. The phylogenetic distribution of serotypes indicated that serotype 4b evolved once from 1/2b, the likely ancestral serotype of lineage I. Serotype 1/2c derived once from 1/2a, with reference strain EGDe (1/2a) likely representing an intermediate evolutionary state. In contrast to housekeeping genes, the virulence factor internalin (InlA) evolved by localized recombination resulting in a mosaic pattern, with convergent evolution indicative of natural selection towards a truncation of InlA protein. This work provides a reference evolutionary framework for future studies on L. monocytogenes epidemiology, ecology, and virulence.

SUBMITTER: Ragon M

PROVIDER: S-EPMC2518857 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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A new perspective on Listeria monocytogenes evolution.

Ragon Marie M Wirth Thierry T Hollandt Florian F Lavenir Rachel R Lecuit Marc M Le Monnier Alban A Brisse Sylvain S

PLoS pathogens 20080905 9

Listeria monocytogenes is a model organism for cellular microbiology and host-pathogen interaction studies and an important food-borne pathogen widespread in the environment, thus representing an attractive model to study the evolution of virulence. The phylogenetic structure of L. monocytogenes was determined by sequencing internal portions of seven housekeeping genes (3,288 nucleotides) in 360 representative isolates. Fifty-eight of the 126 disclosed sequence types were grouped into seven well ...[more]

PMID: 18773117

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Project description:BACKGROUND: While 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. RESULTS: The 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. CONCLUSION: Our 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.

Project description:The occurrence and the antibiogram signatures of Listeria monocytogenes (Lm) recovered from 65 milk samples and its products within the Eastern Cape province were examined. The EN ISO 11290:2017 procedures Parts 1 and 2 described by the International Organization for Standardization for the enumeration and isolation of Lm was adopted for the study. Lm was detected in 18.46% of all the samples examined, and the strains recovered from the samples belong to serotypes 4b and 1/2b. The virulence determinants including prfA, plcA, plcB, inlA, inlC, hly, mpl, actA, inlJ and inlB were detected in all the isolates. About 95.24% of the studied Lm isolates demonstrated potential capacity for biofilm formation. The antibiogram profile revealed high resistance against sulfamethoxazole (71.43%), trimethoprim (52.86%); erythromycin, cefotetan and oxytetracycline (42.86% respectively). About 85.71% exhibited multiple antibiotic resistance phenotypes against the test antibiotics. The resistance determinants encoding resistance against the β-lactamase antibiotics [such as the blaTEM, blaSHV, blaTEM variants (TEM-1 and TEM-2) and the blaZ], the tetracycline resistance genes (including tetA, tetD, tetG and tetM and tetK) were detected among resistant isolates. In addition, the aminoglycoside resistance gene aph (3)-IIa (aphA2)a was detected only in one isolate. Finally, the sulfonamide resistance genes including the sul2 and the sul1 genes were the most frequently observed among Lm isolates. Generally, 71.43% of all Lm isolates recovered from the samples investigated harboured one or more resistance genes encoding resistance against various antibiotics. The antibiogram signatures of Lm isolates observed in this study is an indication that empirical treatment of listeriosis may be challenging in the future as the pathogen may obliterate the success of antibiotics. We, therefore, advocate for the recognition of the One Health approach to ensuring food safety and curbing the spread of antimicrobial resistance in food.

Project description:Listeria monocytogenes is a significant foodborne pathogen causing severe systemic infections in humans with high mortality rates. The objectives of this work were to establish a phylogenetic framework of L. monocytogenes from China and to investigate sequence diversity among different serotypes. We selected 17 L. monocytogenes strains recovered from patients and foods in China representing serotypes 1/2a, 1/2b, and 1/2c. Draft genome sequences were determined using Illumina MiSeq technique and associated protocols. Open reading frames were assigned using prokaryotic genome annotation pipeline by NCBI. Twenty-four published genomes were included for comparative genomic and phylogenetic analysis. More than 154,000 single nucleotide polymorphisms (SNPs) were identified from multiple genome alignment and used to reconstruct maximum likelihood phylogenetic tree. The 41 genomes were differentiated into lineages I and II, which consisted of 4 and 11 subgroups, respectively. A clinical strain from China (SHL009) contained significant SNP differences compared to the rest genomes, whereas clinical strain SHL001 shared most recent common ancestor with strain SHL017 from food. Moreover, clinical strains SHL004 and SHL015 clustered together with two strains (08-5578 and 08-5923) recovered from an outbreak in Canada. Partial sequences of a plasmid found in the Canadian strain were also present in SHL004. We investigated the presence of various genes and gene clusters associated with virulence and subgroup-specific genes, including internalins, L. monocytogenes pathogenicity islands (LIPIs), L. monocytogenes genomic islands (LGIs), stress survival islet 1 (SSI-1), and clustered regularly interspaced short palindromic repeats (CRISPR)/cas system. A novel genomic island, denoted as LGI-2 was identified. Comparative sequence analysis revealed differences among the L. monocytogenes strains related to virulence, survival abilities, and attributes against foreign genetic elements. L. monocytogenes from China were genetically diverse. Strains from clinical specimens and food related closely suggesting foodborne transmission of human listeriosis.

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A new perspective on Listeria monocytogenes evolution.

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A new perspective on Listeria monocytogenes evolution.

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