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Evolutionary and Genomic Microbiology

Investigation of the Relationship between Lactococcal Host Cell Wall Polysaccharide Genotype and 936 Phage Receptor Binding Protein Phylogeny

Jennifer Mahony, Witold Kot, James Murphy, Stuart Ainsworth, Horst Neve, Lars H. Hansen, Knut J. Heller, Søren J. Sørensen, Karin Hammer, Christian Cambillau, Finn K. Vogensen, Douwe van Sinderen
Jennifer Mahony
Department of Microbiology, University College Cork, Cork, Irelanda
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Witold Kot
Department of Food Science, Faculty of Science, University of Copenhagen, Copenhagen, Denmarkb
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James Murphy
Department of Microbiology, University College Cork, Cork, Irelanda
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Stuart Ainsworth
Department of Microbiology, University College Cork, Cork, Irelanda
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Horst Neve
Max Rubner Institut, Kiel, Germanyc
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Lars H. Hansen
Department of Biology, Faculty of Science, University of Copenhagen (KU), Copenhagen, Denmarkd
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Knut J. Heller
Max Rubner Institut, Kiel, Germanyc
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Søren J. Sørensen
Department of Biology, Faculty of Science, University of Copenhagen (KU), Copenhagen, Denmarkd
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Karin Hammer
Department of Systems Biology, Technical University of Denmark, Lyngby, Denmarke
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Christian Cambillau
Architecture et Fonction des Macromolécules Biologiques, UMR 7257 CNRS and Aix-Marseille University, Marseille, Francef
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Finn K. Vogensen
Department of Food Science, Faculty of Science, University of Copenhagen, Copenhagen, Denmarkb
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Douwe van Sinderen
Department of Microbiology, University College Cork, Cork, Irelanda
Alimentary Pharmabiotic Centre, Biosciences Institute, University College Cork, Cork, Irelandg
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DOI: 10.1128/AEM.00653-13
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  • Fig 1
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    Fig 1

    Comparison of the genomic regions encoding the CWPS biosynthesis clusters of six lactococcal strains (UC509.9, CV56, IL1403, KF147, SK11, and MG1363). Homologous protein-encoding genes are joined by gray blocks including the level of identity (percent amino acids) relative to UC509.9. The three subgroups of CWPS are the UC509.9/CV56 (UC/CV) (CWPS A), the IL1403/KF147 (IL/KF) (CWPS B), and the MG1363/SK11 (MG/SK) (CWPS C) subgroups, with unique regions in the operons of UC509.9, IL1403, and MG1363 in the schematic highlighted by stars to indicate the genes upon which the multiplex PCRs are based. The control for the multiplex PCR was based on the rmlB gene, which is conserved in each of the strains.

  • Fig 2
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    Fig 2

    Representative phylogenetic tree of the RBP variable C termini of 32 936 phages, including the 11 sequenced phages of this study. Three major groups of the 936 RBPs are observed: group I includes the majority of phages in this study that infect strains with a MG/SK CWPS (except 936), group II includes those phages in this study that infect strains with an IL/KF CWPS, and group III represents a small group with a divergent RBP that predominantly infects strains with an IL/KF CWPS but also infects a strain with the MG/SK CWPS with equal efficiency.

  • Fig 3
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    Fig 3

    Representative electron micrographs of each of the 11 phages used in this study. The phages are grouped according to the RBP grouping assigned in this study (RBP groups I, II, and III). Where a collar-like structure is observed, it is highlighted with an asterisk in the image.

Tables

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  • Additional Files
  • Table 1

    Features of the lactococcal strains used in this study

    StrainReference or sourceaOrganismCWPS typeInfected by phage(s)
    IL1403 35 L. lactis subsp. lactisIL/KF (B)+
    F7/2 36 L. lactis subsp. lactis biovar diacetylactisIL/KF (B)+
    Bu2-60 37 L. lactis subsp. lactisIL/KF (B)+
    455Dupont-DaniscoL. lactis subsp. cremorisIL/KF (B)+
    UC77UCCL. lactis subsp. cremorisIL/KF (B)+
    229UCCL. lactis subsp. lactisIL/KF (B)−
    WM1UCCL. lactis subsp. lactisUC/CV (A)−
    ML8 1 L. lactis subsp. cremorisUC/CV (A)−
    C10UCCL. lactis subsp. cremorisUC/CV (A)−
    IE-16 1 L. lactis subsp. cremorisUC/CV (A)−
    SMQ-450 1 L. lactis subsp. cremorisUC/CV (A)−
    SMQ-562 1 L. lactis subsp. cremorisUC/CV (A)−
    111 1 L. lactis subsp. cremorisUC/CV (A)−
    UC063UCCL. lactis subsp. cremorisUC/CV (A)−
    UC509.9UCCL. lactis subsp. cremorisUC/CV (A)−
    UL8UCCL. lactis subsp. lactisUC/CV (A)−
    275UCCL. lactis subsp. lactisUC/CV (A)−
    KH 28 L. lactis subsp. cremorisUC/CV (A)−
    C3 38 L. lactis subsp. cremorisUC/CV (A)−
    W22 39 L. lactis subsp. cremorisMG/SK (C)+
    W34 7 L. lactis subsp. cremorisMG/SK (C)+
    3107 40 L. lactis subsp. cremorisMG/SK (C)+
    WG2 36 L. lactis subsp. cremorisMG/SK (C)+
    FD13 9 L. lactis subsp. cremorisMG/SK (C)+
    H2 41 L. lactis subsp. cremorisMG/SK (C)+
    158 34 L. lactis subsp. cremorisMG/SK (C)+
    V32.2 42 L. lactis subsp. cremorisMG/SK (C)+
    JM3UCCL. lactis subsp. cremorisMG/SK (C)+
    JM2UCCL. lactis subsp. cremorisMG/SK (C)+
    1196UCCL. lactis subsp. cremorisMG/SK (C)+
    SMQ86 1 L. lactis subsp. cremorisMG/SK (C)−
    US3 43 L. lactis subsp. cremorisMG/SK (C)−
    E8KUL. lactis subsp. cremorisMG/SK (C)+
    MG1614 44 L. lactis subsp. cremorisMG/SK (C)−
    901-1 40 L. lactis subsp. cremorisMG/SK (C)−
    184UCCL. lactis subsp. lactisUnknown−
    • ↵a UCC, University College Cork.

  • Table 2

    Features of the phages used in this study

    PhageSource or referenceSource locationYr of first report/isolationPropagating hostGenome length (kb)G+C content (%)No. of ORFsRBP group
    fd13KUDenmark2004FD1330.67434.753I
    P113g 9 Germany1986IL140330.79634.158II
    P272 9 Germany1986IL140330.77834.161II
    936 34 New Zealand198415827.30234.549II
    P475Danisco CultoaEuropeUnknown45530.96134.357III
    P680Z. Atamer and J. HinrichsbGermany2009IL140329.63135.149II
    7KUDenmark2004V32.232.38234.257I
    645This studyDenmark2004IL140329.24735.051III
    340This studyDenmark2010IL140332.33734.558III
    ViridusJM2This studyIreland2010JM231.09034.359I
    PastusJM3This studyIreland2010JM328.67434.452I
    • ↵a Danisco Cultor Niebüll GmbH, Niebüll, Germany.

    • ↵b University of Hohenheim, Germany.

  • Table 3

    Primers for CWPS multiplex PCR

    PrimerSequence (5′–3′)Product size (bp)
    IL-KFfwGATTCAGTTGCACGGCCG
    IL-KFrvAGTAAGGGGGCGGATTGTG183
    MG-SKfwAAAGCTCATCTTTCCCCTGTTGT
    MG-SKrvGCACCATAGTCTGGAATAAGACC686
    UC-CVfwGTGCCTATGCTCCGTTAGTC
    UC-CVrvCGAGGGCCAATCTCTTTACC442
    CONfw (control)GTACACTATGTTTATAACAATCATCCAG
    CONrvGCAAACCAGATTCAAAGTCAGTATG891
  • Table 4

    Host range of phages assessed in this studya

    Table 4
    • ↵a In gray-shaded blocks are the phages that group into RBP groups I (7, fd13, JM2, and JM3), II (P680, P113g, P272, and 936), and III (P475, 645, and 340).

Additional Files

  • Figures
  • Tables
  • Files in this Data Supplement:

    • Supplemental file 1 -

      Orf predictions for 936 and representative ORFs on the sequenced phages (Table S1).

      PDF, 224K

    • Supplemental file 2 -

      Multiplex PCR for the detection of conserved regions and differential regions of the CWPS cluster of lactococcal genomes (Fig. S1).

      PDF, 139K

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Investigation of the Relationship between Lactococcal Host Cell Wall Polysaccharide Genotype and 936 Phage Receptor Binding Protein Phylogeny
Jennifer Mahony, Witold Kot, James Murphy, Stuart Ainsworth, Horst Neve, Lars H. Hansen, Knut J. Heller, Søren J. Sørensen, Karin Hammer, Christian Cambillau, Finn K. Vogensen, Douwe van Sinderen
Applied and Environmental Microbiology Jun 2013, 79 (14) 4385-4392; DOI: 10.1128/AEM.00653-13

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Investigation of the Relationship between Lactococcal Host Cell Wall Polysaccharide Genotype and 936 Phage Receptor Binding Protein Phylogeny
Jennifer Mahony, Witold Kot, James Murphy, Stuart Ainsworth, Horst Neve, Lars H. Hansen, Knut J. Heller, Søren J. Sørensen, Karin Hammer, Christian Cambillau, Finn K. Vogensen, Douwe van Sinderen
Applied and Environmental Microbiology Jun 2013, 79 (14) 4385-4392; DOI: 10.1128/AEM.00653-13
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