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Recombination and positive selection contributed to the evolution of Listeria monocytogenes lineages III and IV, two distinct and well supported uncommon L. monocytogenes lineages.

ABSTRACT: Listeriamonocytogenes lineages III and IV represent two uncommon lineages of the human and animal pathogen L. monocytogenes, characterized by occurrence of unusual phenotypic and genetic characteristics that differentiate them from the common lineages I and II. To gain further insights into the evolution of lineages III and IV, we amplified and sequenced housekeeping genes (i.e., gap, prs, purM, ribC, and sigB), internalin genes (i.e., inlA, inlB, inlC, inlG, inlC2, inlD, inlE, inlF, and inlH) and the virulence gene cluster containing prfA, plcA, hly, mpl, actA, and plcB for lineages III (n = 7) and IV (n = 4) isolates. Phylogenetic analyses of the sequences obtained along with previously reported sequence data for 40 isolates representing lineages I (n = 18), II (n = 21), and III (n = 1), showed that lineages III and IV represent divergent and monophyletic lineages. The virulence gene cluster as well as the inlAB operon were present in all isolates, with inlF absent from all lineages III and IV isolates. While all lineage IV isolates contained only inlC (in addition to inlAB), lineage III isolates showed considerable diversity with regard to internalin gene presence, including presence of (i) only inlC (n = 2), (ii) inlC and inlGC2DE (n = 3), (iii) only inlGC2DE (n = 2), and (iv) inlC and inlC2DE (n = 1). In addition to evidence for horizontal gene transfer events, among lineages III and IV isolates, in prs, actA, plcB, mpl, inlA, inlB, inlG, inlD, and inlE, we also found significant evidence for positive selection in the hly promoter region and, along the lineages III and IV branches, for actA (including in sites recognized for interactions with proteins involved in actin tail polymerization). In conclusion, lineages III and IV represent two distinct monophyletic groups with contributions of intragenic recombination to the evolution of their internalin genes as well as contributions of positive selection to evolution of the virulence genes island.

SUBMITTER: Tsai YH

PROVIDER: S-EPMC3224679 | biostudies-literature | 2011 Dec

REPOSITORIES: biostudies-literature

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Recombination and positive selection contributed to the evolution of Listeria monocytogenes lineages III and IV, two distinct and well supported uncommon L. monocytogenes lineages.

Tsai Yeu-Harn Lucy YH Maron Steve B SB McGann Patrick P Nightingale Kendra K KK Wiedmann Martin M Orsi Renato H RH

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases 20110811 8

Listeriamonocytogenes lineages III and IV represent two uncommon lineages of the human and animal pathogen L. monocytogenes, characterized by occurrence of unusual phenotypic and genetic characteristics that differentiate them from the common lineages I and II. To gain further insights into the evolution of lineages III and IV, we amplified and sequenced housekeeping genes (i.e., gap, prs, purM, ribC, and sigB), internalin genes (i.e., inlA, inlB, inlC, inlG, inlC2, inlD, inlE, inlF, and inlH) a ...[more]

PMID: 21854875

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Project description:BackgroundListeria monocytogenes is a food-borne pathogen that causes infections with a high-mortality rate and has served as an invaluable model for intracellular parasitism. Here, we report complete genome sequences for two L. monocytogenes strains belonging to serotype 4a (L99) and 4b (CLIP80459), and transcriptomes of representative strains from lineages I, II, and III, thereby permitting in-depth comparison of genome- and transcriptome -based data from three lineages of L. monocytogenes. Lineage III, represented by the 4a L99 genome is known to contain strains less virulent for humans.ResultsThe genome analysis of the weakly pathogenic L99 serotype 4a provides extensive evidence of virulence gene decay, including loss of several important surface proteins. The 4b CLIP80459 genome, unlike the previously sequenced 4b F2365 genome harbours an intact inlB invasion gene. These lineage I strains are characterized by the lack of prophage genes, as they share only a single prophage locus with other L. monocytogenes genomes 1/2a EGD-e and 4a L99. Comparative transcriptome analysis during intracellular growth uncovered adaptive expression level differences in lineages I, II and III of Listeria, notable amongst which was a strong intracellular induction of flagellar genes in strain 4a L99 compared to the other lineages. Furthermore, extensive differences between strains are manifest at levels of metabolic flux control and phosphorylated sugar uptake. Intriguingly, prophage gene expression was found to be a hallmark of intracellular gene expression. Deletion mutants in the single shared prophage locus of lineage II strain EGD-e 1/2a, the lma operon, revealed severe attenuation of virulence in a murine infection model.ConclusionComparative genomics and transcriptome analysis of L. monocytogenes strains from three lineages implicate prophage genes in intracellular adaptation and indicate that gene loss and decay may have led to the emergence of attenuated lineages.

Project description:In an attempt to develop a method to discriminate among isolates of Listeria monocytogenes, the sequences of all of the annotated genes from the fully sequenced strain L. monocytogenes EGD-e (serotype 1/2a) were compared by BLASTn to a file of the unfinished genomic sequence of L. monocytogenes ATCC 19115 (serotype 4b). Approximately 7% of the matching genes demonstrated 90% or lower identity between the two strains, and the lowest observed identity was 80%. Nine genes (hisJ, cbiE, truB, ribC, comEA, purM, aroE, hisC, and addB) in the 80 to 90% identity group and two genes (gyrB and rnhB) with approximately 97% identity were selected for multilocus sequence analysis in two sets of L. monocytogenes isolates (a 15-strain diversity set and a set of 19 isolates from a single food-processing plant). Based on concatenated sequences, a total of 33 allotypes were differentiated among the 34 isolates tested. Population genetics analyses revealed three lineages of L. monocytogenes that differed in their history of apparent recombination. Lineage I appeared to be completely clonal, whereas representatives of the other lineages demonstrated evidence of horizontal gene transfer and recombination. Although most of the gene sequences for lineage II strains were distinct from those of lineage I, a few strains with the majority of genes characteristic of lineage II had some that were characteristic of lineage I. Genes from lineage III organisms were mostly similar to lineage I genes, with instances of genes appearing to be mosaics with lineage II genes. Even though lineage I and lineage II generally demonstrated very distinct sequences, the sequences for the 11 selected genes demonstrated little discriminatory power within each lineage. In the L. monocytogenes isolate set obtained from one food-processing plant, lineage I and lineage II were found to be almost equally prevalent. While it appears that different lineages of L. monocytogenes can share habitats, they appear to differ in their histories of horizontal gene transfer.

Project description:BackgroundThe bacterium Listeria monocytogenes is a saprotroph as well as an opportunistic human foodborne pathogen, which has previously been shown to consist of at least two widespread lineages (termed lineages I and II) and an uncommon lineage (lineage III). While some L. monocytogenes strains show evidence for considerable diversification by homologous recombination, our understanding of the contribution of recombination to L. monocytogenes evolution is still limited. We therefore used STRUCTURE and ClonalFrame, two programs that model the effect of recombination, to make inferences about the population structure and different aspects of the recombination process in L. monocytogenes. Analyses were performed using sequences for seven loci (including the house-keeping genes gap, prs, purM and ribC, the stress response gene sigB, and the virulence genes actA and inlA) for 195 L. monocytogenes isolates.ResultsSequence analyses with ClonalFrame and the Sawyer's test showed that recombination is more prevalent in lineage II than lineage I and is most frequent in two house-keeping genes (ribC and purM) and the two virulence genes (actA and inlA). The relative occurrence of recombination versus point mutation is about six times higher in lineage II than in lineage I, which causes a higher genetic variability in lineage II. Unlike lineage I, lineage II represents a genetically heterogeneous population with a relatively high proportion (30% average) of genetic material imported from external sources. Phylograms, constructed with correcting for recombination, as well as Tajima's D data suggest that both lineages I and II have suffered a population bottleneck.ConclusionOur study shows that evolutionary lineages within a single bacterial species can differ considerably in the relative contributions of recombination to genetic diversification. Accounting for recombination in phylogenetic studies is critical, and new evolutionary models that account for the possibility of changes in the rate of recombination would be required. While previous studies suggested that only L. monocytogenes lineage I has experienced a recent bottleneck, our analyses clearly show that lineage II experienced a bottleneck at about the same time, which was subsequently obscured by abundant homologous recombination after the lineage II bottleneck. While lineage I and lineage II should be considered separate species from an evolutionary viewpoint, maintaining single species name may be warranted since both lineages cause the same type of human disease.

Dataset Information

Recombination and positive selection contributed to the evolution of Listeria monocytogenes lineages III and IV, two distinct and well supported uncommon L. monocytogenes lineages.

Publications

Recombination and positive selection contributed to the evolution of Listeria monocytogenes lineages III and IV, two distinct and well supported uncommon L. monocytogenes lineages.

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