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Research Article | Host-Microbe Biology

Genomic Epidemiology and Evolution of Escherichia coli in Wild Animals in Mexico

Robert Murphy, Martin Palm, Ville Mustonen, Jonas Warringer, Anne Farewell, Leopold Parts, Danesh Moradigaravand
Maria L. Marco, Editor
Robert Murphy
aUniversity of Copenhagen, Department of Biology, Section for Ecology and Evolution, Copenhagen, Denmark
bCenter for Computational Biology, Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, United Kingdom
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Martin Palm
cDepartment for Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
dCentre for Antibiotic Resistance Research at the University of Gothenburg, Gothenburg, Sweden
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  • ORCID record for Martin Palm
Ville Mustonen
eOrganismal and Evolutionary Biology Research Programme, Department of Computer Science, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
fHelsinki Institute for Information Technology, Helsinki, Finland
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Jonas Warringer
cDepartment for Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
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Anne Farewell
cDepartment for Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
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Leopold Parts
gWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom
hDepartment of Computer Science, University of Tartu, Tartu, Estonia
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Danesh Moradigaravand
bCenter for Computational Biology, Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, United Kingdom
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  • ORCID record for Danesh Moradigaravand
Maria L. Marco
University of California, Davis
Roles: Editor
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DOI: 10.1128/mSphere.00738-20
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  • FIG 1
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    FIG 1

    Phylogenetic distribution of host specificity and cluster analysis. (A) Phylogenetic tree of our E. coli strains from wild-animal hosts and its association with host taxonomy, at different taxonomic levels. Families of host species colonized by only one E. coli strain in our collection are not shown. (B) Principal-component analysis of our E. coli strains, with labels representing the phylogroup of the E. coli isolate and the taxonomic rank of the host species. Each color corresponds to one taxonomic rank, shown in panel A. (C) Distribution of pairwise SNP distances for E. coli strains from hosts belonging to the same (red) and different (blue) taxonomic ranks.

  • FIG 2
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    FIG 2

    Concordance between host and E. coli phylogenetic trees. (A) Phylogenetic tree of the whole-genome sequencing of E. coli strains and the tree of life (TOL) for host strains. For host species for which more than one isolate were available in the data set, one strain was randomly drawn. Clades for bird and major mammalian orders are highlighted. (B) The frequency (y axis) of path tree differences relative to the E. coli tree (x axis) for 1,000 random shuffling of tree tips of the host tree in panel A (black bars), contrasted to the observed value from unpermuted data (red dashed line).

  • FIG 3
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    FIG 3

    Recent mixing of wild and nonwild host lineages. Bayesian tree for strains in a clade belonging to phylogroup B1. The shaded boxes show putative host jump events between wild hosts and other sites, i.e., domesticated animals, environment, and humans, over the past 100 years. The error bar shows the 95% confidence interval from the Bayesian tree.

  • FIG 4
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    FIG 4

    Distribution of virulence factor genes. (A) Frequency of virulence factors genes across functional groups and taxonomic orders. (B) Phylogenetic distribution of E. coli virulence genes across wild animal host species. The tree shows the tree of life for hosts, where major orders are shown in shaded boxes. Bar plots show the frequency of genes. Horizontal box plots represent the distribution of virulence genes for strains recovered from each host across host orders.

  • FIG 5
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    FIG 5

    Sharing of serotypes and distribution of LEE genes and effectors genes across hosts. (A) Distribution of serotypes shared between E. coli isolates colonizing wild hosts and known pathovars across taxonomic orders of hosts. (B) Distribution of typed and nontyped LEE families across taxonomic orders of hosts. (C) Distribution of virulence genes and LEE effector genes in typed LEE-positive, untyped LEE-positive, and LEE-negative strains.

Supplemental Material

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  • FIG S1

    Phylogeny of E. coli from wild hosts with strains from other sources. (A) Alignment-free phylogenetic tree for the E. coli strains in the context of previously sequenced genomes in the Enterobase database and the associated metadata of phylogroup and isolation sites. (B) The distributions of continent of isolation and host in the curated dataset, compared with those in the Enterobase collection. Accession number and metadata for strains are provided in Table S2. Download FIG S1, TIF file, 0.9 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    Comparison between core genome and accessory genome trees. The core genome and accessory genome trees were reconstructed from the SNPs in the core genome alignment and from the pattern of gene presence and absence, respectively. Download FIG S2, TIF file, 0.7 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    Positive selection analysis. (A) The distribution of functional classifications for 256 genes that were under positive selection, compared with the baseline distribution in the pan genome. We excluded genes without assigned COG group. The letters S, G, P, C, H, and T represent unknown functions, carbohydrate metabolism and transport, inorganic ion transport and metabolism, energy production and conversion, coenzyme metabolism, and signal transduction, respectively. The full interpretation for other classes is found in reference 61. The asterisk sign shows 0.05 significance from Student’s t-test to assess the significance of the difference between groups. (B) Distribution of genes under positive selection across taxonomic host orders. Download FIG S3, TIF file, 0.5 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1

    Samples specification, serotypes, associated pathovars, and virulence and AMR genes for our strains and accession numbers for external strains from wild hosts in Mexico, retrieved from NCBI. Download Table S1, CSV file, 0.1 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4

    Correlation between virulence factor counts and physiological and ecological attributes of wild hosts. (A) Correlation coefficient between the number of virulence genes and ecological features in the panTHERIA dataset. The size and color of the circles correspond to the absolute value and direction of Spearman’s rank correlation coefficient, respectively. Entries with insignificant correlation correlations, i.e., P values of <0.05, are shown as blanks. The red box shows the ecological features that are significantly correlated with virulence factor counts. (B) Correlation between social group size and total number of virulence genes for the wild-host E. coli sample set. The blue line is the fitted linear regression model. The grey area corresponds to the 95% confidence interval. The coefficient is 0.22419, with a standard deviation of 0.09071. (C) Social group size values across host orders. Download FIG S4, TIF file, 0.6 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S5

    Phylogenetic distribution of antimicrobial resistance genes.: The tree was built from SNPs in the core genome, using the neighbor-joining method. For ciprofloxacin resistance, chromosomal mutations are shown. Download FIG S5, TIF file, 0.5 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    Sample specification and associated metadata for external isolates from Enterobase, shown in Fig. S1. Download Table S2, CSV file, 0.1 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S3

    Ka/Ks values and functional annotations for genes present in >70% of isolates. Download Table S3, CSV file, 0.2 MB.

    Copyright © 2021 Murphy et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Genomic Epidemiology and Evolution of Escherichia coli in Wild Animals in Mexico
Robert Murphy, Martin Palm, Ville Mustonen, Jonas Warringer, Anne Farewell, Leopold Parts, Danesh Moradigaravand
mSphere Jan 2021, 6 (1) e00738-20; DOI: 10.1128/mSphere.00738-20

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Genomic Epidemiology and Evolution of Escherichia coli in Wild Animals in Mexico
Robert Murphy, Martin Palm, Ville Mustonen, Jonas Warringer, Anne Farewell, Leopold Parts, Danesh Moradigaravand
mSphere Jan 2021, 6 (1) e00738-20; DOI: 10.1128/mSphere.00738-20
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    • ABSTRACT
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KEYWORDS

Escherichia coli
genomic epidemiology
host-pathogen interaction
infectious diseases
whole-genome sequencing
wild animals

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