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Evolutionary and Genomic Microbiology | Spotlight

Genetic Stability and Evolution of the sigB Allele, Used for Listeria Sensu Stricto Subtyping and Phylogenetic Inference

Jingqiu Liao, Martin Wiedmann, Jasna Kovac
Christopher A. Elkins, Editor
Jingqiu Liao
aDepartment of Food Science, Cornell University, Ithaca, New York, USA
bGraduate Field of Microbiology, Cornell University, Ithaca, New York, USA
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Martin Wiedmann
aDepartment of Food Science, Cornell University, Ithaca, New York, USA
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Jasna Kovac
aDepartment of Food Science, Cornell University, Ithaca, New York, USA
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Christopher A. Elkins
FDA Center for Food Safety and Applied Nutrition
Roles: Editor
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DOI: 10.1128/AEM.00306-17
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  • FIG 1
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    FIG 1

    Phylogenetic trees inferred by the maximum likelihood method using sigB genes of 164 Listeriasensu stricto allelic types (a) and L. monocytogenes lineage I, II, and III isolates (b). Both trees were rooted by midpoint. For the phylogeny shown in panel a, the HKY substitution model with invariable sites and a gamma distribution (HKY+I+G substitution model) was used for constructing the tree with 1,000 bootstrap repetitions. Only bootstrap values of >70% are presented on the tree. L. monocytogenes is indicated in red, L. marthii is in brown, L. innocua is in green, L. welshimeri is in yellow, L. seeligeri is in blue, and L. ivanovii is in purple. For panel b, the GTR+G substitution model was used for constructing the tree with 1,000 bootstrap repetitions; only bootstrap values of >70% are presented in this tree. L. monocytogenes lineage I is indicated by triangles, lineage II is indicated by squares, and lineage III is indicated by circles.

  • FIG 2
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    FIG 2

    Phylogenetic tree inferred by the maximum likelihood method using the core genome SNPs of 21 Listeriasensu stricto isolates. kSNP2 with kmer size of 19 was used to identify core genome SNPs that were used for constructing the tree with the GTR+G substitution model and 1,000 bootstrap repetitions. The tree is rooted by the midpoint. Only bootstrap values of >70% are presented on the tree. L. monocytogenes is indicated in red, L. marthii is in brown, L. innocua is in green, L. welshimeri is in yellow, L. seeligeri is in blue, and L. ivanovii is in purple.

Tables

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  • Additional Files
  • TABLE 1

    Descriptive analysis of nucleotide sequence data for the 660-bp sigB fragment

    Taxon (no. of sequences)No. of:G+C content (%)πbkcTajima's D valuedNo. of mutationsedN/dS ratiof
    HaplotypesaPolymorphic sitesMutationsSynNonsyn
    Listeria sensu stricto (4,280)16018125538.00.07548.9531.944NANA0.011
    L. seeligeri (667)23495138.30.01711.2391.5244920.013
    L. welshimeri (565)37303036.90.0032.041−1.3742460.027
    L. innocua (1,226)41333537.30.0106.8691.2793050.044
    L. ivanovii (12)4252539.60.0159.8790.8612320.017
    L. marthii (14)6171737.20.0117.4181.5991700.000
    L. monocytogenes (1,796)509410338.90.02214.5150.372NANA0.017
    Lineage I (1,032)10131338.90.0042.452−0.8851300.000
    Lineage II (692)12343538.80.0010.757−2.2063140.033
    Lineage III (59)24262638.70.0053.571−1.1602330.020
    Lineage IV (13)43338.70.0010.462−1.652300.000
    • ↵a Sites with gaps are excluded in DnaSP, which was used to determine the number of haplotypes; as AT103, AT154, and AT165 have deletions in their sequences (2, 1, and 3 nucleotides, respectively), the number of Listeriasensu stricto haplotypes (n = 160) is less than the number of ATs (n = 164).

    • ↵b Average pairwise nucleotide diversity per site.

    • ↵c Average number of pairwise nucleotide differences per sequence.

    • ↵d Tajima's D values significantly different from 0 are marked in boldface type.

    • ↵e Syn indicates the number of synonymous mutations; Nonsyn indicates the number of nonsynonymous mutations. If the number of synonymous or nonsynonymous mutations could not be unambiguously inferred, e.g., in highly divergent populations where there are multiple mutations per site, the result is reported as NA (not available).

    • ↵f The ratio of nonsynonymous substitutions per nonsynonymous site to synonymous substitutions per synonymous site. The dN/dS ratio was calculated based on the average dN and dS values obtained by pairwise comparisons of sequences using approximate methods.

  • TABLE 2

    Putative recombination events inferred by RDP4 and PHI testa

    TaxonRecombination determined by RDP4P value for recombination determined by PHI testb
    Recombinant sequencePutative parental sequence (minor × major donor)Detection method(s)
    Listeria sensu stricto L. monocytogenes AT 98 L. marthii AT 143 × L. monocytogenes AT 83Maxchi0.930
    L. monocytogenes AT 151
    L. innocua AT 141 L. monocytogenes AT 75 × L. innocua AT 139SiScan
    L. seeligeri L. seeligeri AT 9 L. seeligeri AT 68 × L. seeligeri AT 92Maxchi0.980
    L. welshimeri 0.750
    L. innocua L. innocua AT 124 L. innocua AT 139 × L. innocua AT 87Bootscan, SiScan, 3Seq 0.002
    L. innocua AT 33
    L. ivanovii 1.000
    L. marthii L. marthii AT 143 L. marthii AT 95 × L. marthii AT 18Bootscan, Maxchi, LARD0.440
    L. monocytogenes 0.297
    Lineage I 0.045
    Lineage II 1.000
    Lineage III 0.440
    Lineage IV NA
    • ↵a Recco did not detect any significant recombination events.

    • ↵b P value of <0.01 is marked in boldface type; NA (not available) indicates that too few informative characters were present in a given taxon.

  • TABLE 3

    Results of positive selection analysis using PAML

    TaxonLn L M1aaLn L M2abSignificance value for comparison of Ln L M1a and Ln L M2acLn L M7aLn L M8bSignificance value for comparison of Ln L M7 and Ln L M8c
    Listeria sensu stricto −3,692.729−3,692.7270.998−3,685.556−3,686.6920.321
    L. seeligeri −1,198.649−1,198.6491.000−1,198.655−1,198.6551.000
    L. welshimeri −1,138.146−1,138.1461.000−1,138.166−1,138.1661.000
    L. innocua −1,354.596−1,353.3140.277−1,354.272−1,352.9910.278
    L. ivanovii −956.510−956.5101.000−956.511−956.5111.000
    L. marthii −958.010−958.0090.999−958.009−958.0100.999
    L. monocytogenes −1,521.006−1,521.0060.999−1,521.934−1,521.0470.412
    Lineage I−947.277−947.2761.000−947.276−947.2771.000
    Lineage II−1,046.284−1,046.2831.000−1,046.289−1,045.3900.407
    Lineage III−1,057.886−1,058.3570.625−1,057.889−1,057.8891.000
    Lineage IV−872.673−872.6731.000−872.673−872.6731.000
    • ↵a Ln L M1a and Ln L M7, log-normal likelihood scores for the null hypothesis that the data set evolved following a neutral model.

    • ↵b Ln L M2a and Ln L M8, log-normal likelihood scores for the alternative hypothesis that the data set evolved under positive selection.

    • ↵c The test statistic was calculated as 2[(−Ln L M1a) − (−Ln L M2a)] and 2[(−Ln L M7) − (−Ln L M8)].

  • TABLE 4

    Molecular evolution parameters for sigB

    TaxonDNA substitution modelati/tv ratiobAlphacP-invd
    Listeria sensu stricto HKY+I+G3.370.900.61
    L. seeligeri TrN+I 0.76
    L. welshimeri HKY+I4.24 0.90
    L. innocua HKY+I+G2.590.530.90
    L. ivanovii HKY7.91
    L. marthii HKY+I11.32 0.94
    L. monocytogenes TrN+G 0.22
    Lineage IHKY+I2.35 0.93
    Lineage IIHKY2.31
    Lineage IIITrN+I 0.81
    Lineage IVHKYNA
    • ↵a HKY, Hasegawa-Kishino-Yano model; I, invariable sites; G, gamma distribution; TrN, Tamura-Nei model.

    • ↵b Ratio of transitions (ti) to transversions (tv). If the ratio could not be unambiguously inferred, the result is reported as NA (not available); this is reported only for the HKY model since the TrN model uses variable transition rates.

    • ↵c The alpha parameter defines the shape of the gamma distribution; this is reported only if the DNA substitution model includes a gamma distribution.

    • ↵d Proportion of invariable sites; this is reported only if the DNA substitution model includes an invariable-site parameter.

  • TABLE 5

    Test of the molecular clock

    TaxonLn L clockaLn L no clockbSignificancecMolecular clock conclusiond
    Detected by PAUP*
        Listeriasensu stricto−2,911.235−2,750.1820.000Reject
        L. seeligeri−1,345.168−1,302.7990.000Reject
        L. welshimeri−1,232.536−1,215.1590.480Fail to reject
        L. innocua−1,524.065−1,474.7040.000Reject
        L. ivanovii−1,055.664−1,026.3370.000Reject
        L. marthii−1,034.063−1,025.0770.001Reject
        L. monocytogenes−1,837.100−1,713.5370.000Reject
        Lineage I−1,026.237−1,015.1450.008Reject
        Lineage II−1,150.381−1,108.5750.000Reject
        Lineage III−1,154.203−1,136.7410.039Reject
        Lineage IV−915.453−914.6520.449Fail to reject
    Detected by PAML
        Listeriasensu stricto−2,699.124−2,544.6630.000Reject
        L. seeligeri−1,331.701−1,289.1920.000Reject
        L. welshimeri−1,230.322−1,213.3130.515Fail to reject
        L. innocua−1,450.986−1,401.4170.000Reject
        L. ivanovii−1,042.710−1,014.4960.000Reject
        L. marthii−1,031.025−1,022.0560.001Reject
        L. monocytogenes−1,791.820−1,666.5010.000Reject
        Lineage I−1,016.090−1,005.9580.016Reject
        Lineage II−1,150.315−1,108.8820.000Reject
        Lineage III−1,141.821−1,123.1960.022Reject
        Lineage IV−914.253−913.4460.446Fail to reject
    • ↵a Ln L clock, log-normal likelihood score for the null hypotheses that the data set evolved following a molecular clock.

    • ↵b Ln L clock, log-normal likelihood score for the alternative hypotheses that the data set did not evolve following a molecular clock.

    • ↵c The test statistic for the molecular clock was calculated as 2[(−Ln L clock) − (−Ln L no clock)].

    • ↵d Conclusion to reject or fail to reject the null hypothesis.

Additional Files

  • Figures
  • Tables
  • Supplemental material

    • Supplemental file 1 -

      Codon usage bias (Table S1), tree topology tests (Table S2), additional recombination analysis (Table S3), accession numbers of 21 whole-genome sequences (Table S4), rearranged tree topology (Fig. S1), and optimal tree topology (Fig. S2).

      PDF, 162K

    • Supplemental file 2 -

      Metadata for 1,420 isolates and 164 sigB AT representative isolates used in this study (Data Set S1).

      XLSX, 154K

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Genetic Stability and Evolution of the sigB Allele, Used for Listeria Sensu Stricto Subtyping and Phylogenetic Inference
Jingqiu Liao, Martin Wiedmann, Jasna Kovac
Applied and Environmental Microbiology May 2017, 83 (12) e00306-17; DOI: 10.1128/AEM.00306-17

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Genetic Stability and Evolution of the sigB Allele, Used for Listeria Sensu Stricto Subtyping and Phylogenetic Inference
Jingqiu Liao, Martin Wiedmann, Jasna Kovac
Applied and Environmental Microbiology May 2017, 83 (12) e00306-17; DOI: 10.1128/AEM.00306-17
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    • ABSTRACT
    • INTRODUCTION
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KEYWORDS

Bacterial Proteins
Bacterial Typing Techniques
Evolution, Molecular
Listeria
phylogeny
sigma factor
sigB
homologous recombination
positive selection
molecular clock
allelic typing

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