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Bacteriophage replication requires specific host-recognition. Some siphophages harbour a large complex, the baseplate, at the tip of their non-contractile tail. This baseplate holds receptor binding proteins (RBPs) that can recognize the host cell-wall polysaccharide (CWPS) and specifically attach the phage to its host. While most phages possess a dedicated RBP, the phage J-1 that infects Lactobacillus casei seemed to lack one. It has been shown that the phage J-1 distal tail protein (Dit) plays a role in host recognition and that its sequence comprises two inserted modules compared with ‘classical’ Dits. The first insertion is similar to carbohydrate-binding modules (CBMs), whereas the second insertion remains undocumented. Here, we determined the structure of the second insertion and found it also similar to several CBMs. Expressed insertion CBM2, but not CBM1, binds to L. casei cells and neutralize phage attachment to the bacterial cell wall and the isolated and purified CWPS of L. casei BL23 prevents CBM2 attachment to the host. Electron microscopy single particle reconstruction of the J-1 virion baseplate revealed that CBM2 is projected at the periphery of Dit to optimally bind the CWPS receptor. Taken together, these results identify J-1 evolved Dit as the phage RBP. © 2017 John Wiley & Sons Ltd


Documento: Artículo
Título:Evolved distal tail carbohydrate binding modules of Lactobacillus phage J-1: a novel type of anti-receptor widespread among lactic acid bacteria phages
Autor:Dieterle, M.-E.; Spinelli, S.; Sadovskaya, I.; Piuri, M.; Cambillau, C.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IQUIBICEN-CONICET, Buenos Aires, Argentina
Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS), Campus de Luminy, Case 932, Marseille Cedex 09, 13288, France
Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université (AMU), Campus de Luminy, Case 932, Marseille Cedex 09, 13288, France
Université Lille Nord de France, Lille, F-59000, France
Université du Littoral-Côte d'Opale, LR2B/UMT 08, Bassin Napoléon, BP 120, Boulogne-sur-Mer Cedex, F-62327, France
Palabras clave:carbohydrate binding protein; carbohydrate; lactic acid; protein binding; viral protein; amino terminal sequence; Article; bacterial cell wall; bacterial strain; bacteriophage; bacterium isolate; controlled study; electron microscopy; lactic acid bacterium; Lactobacillus casei; nonhuman; priority journal; protein binding; protein domain; protein expression; protein folding; virion; bacteriophage; genetics; host range; Lactobacillus; Lactobacillus casei; Lactococcus lactis; metabolism; protein conformation; structure activity relation; ultrastructure; Bacteriophages; Carbohydrates; Host Specificity; Lactic Acid; Lactobacillus; Lactobacillus casei; Lactococcus lactis; Microscopy, Electron; Protein Binding; Protein Conformation; Structure-Activity Relationship; Viral Tail Proteins; Virion
Página de inicio:608
Página de fin:620
Título revista:Molecular Microbiology
Título revista abreviado:Mol. Microbiol.
CAS:lactic acid, 113-21-3, 50-21-5; Carbohydrates; Lactic Acid; Viral Tail Proteins


  • Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., PHENIX: a comprehensive Python-based system for macromolecular structure solution (2010) Acta Crystallogr D Biol Crystallogr, 66, pp. 213-221
  • Ainsworth, S., Sadovskaya, I., Vinogradov, E., Courtin, P., Guerardel, Y., Mahony, J., Differences in lactococcal cell wall polysaccharide structure are major determining factors in bacteriophage sensitivity (2014) MBio, 5, pp. e00814-e00880. , e
  • Aslanidis, C., de Jong, P.J., Ligation-independent cloning of PCR products (LIC-PCR) (1990) Nucleic Acids Res, 18, pp. 6069-6074
  • Bebeacua, C., Bron, P., Lai, L., Vegge, C.S., Brondsted, L., Spinelli, S., Structure and molecular assignment of lactococcal phage TP901-1 baseplate (2010) J Biol Chem, 285, pp. 39079-39086
  • Blanc, E., Roversi, P., Vonrhein, C., Flensburg, C., Lea, S.M., Bricogne, G., Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT (2004) Acta Crystallogr D Biol Crystallogr, 60, pp. 2210-2221
  • Capra, M.L., Quiberoni, A., Reinheimer, J., Phages of Lactobacillus casei/paracasei: response to environmental factors and interaction with collection and commercial strains (2006) J Appl Microbiol, 100, pp. 334-342
  • De la Rosa-Trevin, J.M., Oton, J., Marabini, R., Zaldivar, A., Vargas, J., Carazo, J.M., Sorzano, C.O., Xmipp 3.0: an improved software suite for image processing in electron microscopy (2013) J Struct Biol, 184, pp. 321-328
  • Desmyter, A., Farenc, C., Mahony, J., Spinelli, S., Bebeacua, C., Blangy, S., Viral infection modulation and neutralization by camelid nanobodies (2013) Proc Natl Acad Sci U S A, 110, pp. E1371-E1379
  • Dieterle, M.E., Bowman, C., Batthyany, C., Lanzarotti, E., Turjanski, A., Hatfull, G., Piuri, M., Exposing the secrets of two well-known Lactobacillus casei phages, J-1 and PL-1, by genomic and structural analysis (2014) Appl Environ Microbiol, 80, pp. 7107-7121
  • Dieterle, M.E., Jacobs-Sera, D., Russell, D., Hatfull, G., Piuri, M., Complete genome sequences of Lactobacillus Phages J-1 and PL-1 (2014) Genome Announc, 2
  • Dieterle, M.E., Fina Martin, J., Duran, R., Nemirovsky, S.I., Sanchez Rivas, C., Bowman, C., Characterization of prophages containing ‘evolved’ Dit/Tal modules in the genome of Lactobacillus casei BL23 (2016) Appl Microbiol Biotechnol, 100, pp. 9201-9215
  • Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot (2010) Acta Crystallogr D Biol Crystallogr, 66, pp. 486-501
  • Farenc, C., Spinelli, S., Vinogradov, E., Tremblay, D., Blangy, S., Sadovskaya, I., Moineau, S., Cambillau, C., Molecular insights on the recognition of a Lactococcus lactis cell wall pellicle by the phage 1358 receptor binding protein (2014) J Virol, 88, pp. 7005-7015
  • Flayhan, A., Vellieux, F.M., Lurz, R., Maury, O., Contreras-Martel, C., Girard, E., Boulanger, P., Breyton, C., Crystal structure of pb9, the distal tail protein of bacteriophage t5: a conserved structural motif among all siphophages (2014) J Virol, 88, pp. 820-828
  • Goulet, A., Lai-Kee-Him, J., Veesler, D., Auzat, I., Robin, G., Shepherd, D.A., The opening of the SPP1 bacteriophage tail, a prevalent mechanism in Gram-positive-infecting siphophages (2011) J Biol Chem, 286, pp. 25397-25405
  • Hino Mai, N., Lactic Acid Bacteria employed for beverage production. II. Isolation and some properties of a bacteriophage isolated during the fermentation of lactic acid beverage (1965) J Chem Soc Jpn, 39, pp. 472-476
  • Holm, L., Kaariainen, S., Rosenstrom, P., Schenkel, A., Searching protein structure databases with DaliLite v.3 (2008) Bioinformatics, 24, pp. 2780-2781
  • Hudson, K.L., Bartlett, G.J., Diehl, R.C., Agirre, J., Gallagher, T., Kiessling, L.L., Woolfson, D.N., Carbohydrate-aromatic interactions in proteins (2015) J Am Chem Soc, 137, pp. 15152-15160
  • Kabsch, W., XDS (2010) Acta Crystallogr D Biol Crystallogr, 66, pp. 125-132
  • Kanamaru, S., Leiman, P.G., Kostyuchenko, V.A., Chipman, P.R., Mesyanzhinov, V.V., Arisaka, F., Rossmann, M.G., Structure of the cell-puncturing device of bacteriophage T4 (2002) Nature, 415, pp. 553-557
  • Kostyuchenko, V.A., Leiman, P.G., Chipman, P.R., Kanamaru, S., van Raaij, M.J., Arisaka, F., Mesyanzhinov, V.V., Rossmann, M.G., Three-dimensional structure of bacteriophage T4 baseplate (2003) Nat Struct Biol, 10, pp. 688-693
  • Legrand, P., Collins, B., Blangy, S., Murphy, J., Spinelli, S., Gutierrez, C., The atomic structure of the phage tuc2009 baseplate tripod suggests that host recognition involves two different carbohydrate binding modules (2016) MBio, 7, p. 15
  • Mahony, J., Kot, W., Murphy, J., Ainsworth, S., Neve, H., Hansen, L.H., Investigation of the relationship between lactococcal host cell wall polysaccharide genotype and 936 phage receptor binding protein phylogeny (2013) Appl Environ Microbiol, 79, pp. 4385-4392
  • Mahony, J., McDonnell, B., Casey, E., van Sinderen, D., Phage-host interactions of cheese-making lactic acid bacteria (2016) Annu Rev Food Sci Technol, 7, pp. 267-285
  • Mahony, J., Oliveira, J., Collins, B., Haanemaaijer, L., Lugli, G.A., Neve, H., Genetic and functional characterisation of the lactococcal P335 phage-host interactions (2017) BMC Genom, 18, p. 146
  • Murphy, J., Bottacini, F., Mahony, J., Kelleher, P., Neve, H., Zomer, A., Nauta, A., van Sinderen, D., Comparative genomics and functional analysis of the 936 group of lactococcal Siphoviridae phages (2016) Sci Rep, 6, p. 21345
  • Otwinowski, Z., DENZO: oscillation data and reducing program (1993) Data Collection and Processing, , In, Sawyer, L., Isaacs, N.W., Bailey, S., (eds)., Warrington, UK, SERC Daresbury Laboratory
  • Pape, T., Schneider, T.R., HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs (2004) J Appl Crystallogr, 37, pp. 844-853
  • Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera–a visualization system for exploratory research and analysis (2004) J Comput Chem, 25, pp. 1605-1612
  • Scheres, S.H., Nunez-Ramirez, R., Sorzano, C.O., Carazo, J.M., Marabini, R., Image processing for electron microscopy single-particle analysis using XMIPP (2008) Nat Protoc, 3, pp. 977-990
  • Sciara, G., Bebeacua, C., Bron, P., Tremblay, D., Ortiz-Lombardia, M., Lichiere, J., Structure of lactococcal phage p2 baseplate and its mechanism of activation (2010) Proc Natl Acad Sci U S A, 107, pp. 6852-6857
  • Sheldrick, G.M., A short history of SHELX (2008) Acta Crystallogr A, 64, pp. 112-122
  • Soding, J., Biegert, A., Lupas, A.N., The HHpred interactive server for protein homology detection and structure prediction (2005) Nucleic Acids Res, 33, pp. W244-W248
  • Sorzano, C.O., Marabini, R., Velazquez-Muriel, J., Bilbao-Castro, J.R., Scheres, S.H., Carazo, J.M., Pascual-Montano, A., XMIPP: a new generation of an open-source image processing package for electron microscopy (2004) J Struct Biol, 148, pp. 194-204
  • Spinelli, S., Desmyter, A., Verrips, C.T., de Haard, H.J., Moineau, S., Cambillau, C., Lactococcal bacteriophage p2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses (2006) Nat Struct Mol Biol, 13, pp. 85-89
  • Spinelli, S., Veesler, D., Bebeacua, C., Cambillau, C., Structures and host-adhesion mechanisms of lactococcal siphophages (2014) Front Microbiol, 5, p. 3
  • Taylor, N.M., Prokhorov, N.S., Guerrero-Ferreira, R.C., Shneider, M.M., Browning, C., Goldie, K.N., Stahlberg, H., Leiman, P.G., Structure of the T4 baseplate and its function in triggering sheath contraction (2016) Nature, 533, pp. 346-352
  • Unger, T., Jacobovitch, Y., Dantes, A., Bernheim, R., Peleg, Y., Applications of the Restriction Free (RF) cloning procedure for molecular manipulations and protein expression (2010) J Struct Biol, 172, pp. 34-44
  • Vagin, A., Teplyakov, A., Molecular replacement with MOLREP (2010) Acta Crystallogr D Biol Crystallogr, 66, pp. 22-25
  • Veesler, D., Cambillau, C., A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries (2011) Microbiol Mol Biol Rev, 75, pp. 423-433
  • Veesler, D., Robin, G., Lichiere, J., Auzat, I., Tavares, P., Bron, P., Campanacci, V., Cambillau, C., Crystal structure of bacteriophage spp1 distal tail protein (gp19.1): a baseplate hub paradigm in gram-positive infecting phages (2010) J Biol Chem, 285, pp. 36666-36673
  • Veesler, D., Spinelli, S., Mahony, J., Lichiere, J., Blangy, S., Bricogne, G., Structure of the phage TP901-1 1.8 MDa baseplate suggests an alternative host adhesion mechanism (2012) Proc Natl Acad Sci U S A, 109, pp. 8954-8958
  • Vinogradov, E., Sadovskaya, I., Grard, T., Chapot-Chartier, M.P., Structural studies of the rhamnose-rich cell wall polysaccharide of Lactobacillus casei BL23 (2016) Carbohydr Res, 435, pp. 156-161
  • Yokokura, T., Phage receptor material in Lactobacillus casei cell wall. I. Effect of L-rhamnose on phage adsorption to the cell wall (1971) Jpn J Microbiol, 15, pp. 457-463


---------- APA ----------
Dieterle, M.-E., Spinelli, S., Sadovskaya, I., Piuri, M. & Cambillau, C. (2017) . Evolved distal tail carbohydrate binding modules of Lactobacillus phage J-1: a novel type of anti-receptor widespread among lactic acid bacteria phages. Molecular Microbiology, 104(4), 608-620.
---------- CHICAGO ----------
Dieterle, M.-E., Spinelli, S., Sadovskaya, I., Piuri, M., Cambillau, C. "Evolved distal tail carbohydrate binding modules of Lactobacillus phage J-1: a novel type of anti-receptor widespread among lactic acid bacteria phages" . Molecular Microbiology 104, no. 4 (2017) : 608-620.
---------- MLA ----------
Dieterle, M.-E., Spinelli, S., Sadovskaya, I., Piuri, M., Cambillau, C. "Evolved distal tail carbohydrate binding modules of Lactobacillus phage J-1: a novel type of anti-receptor widespread among lactic acid bacteria phages" . Molecular Microbiology, vol. 104, no. 4, 2017, pp. 608-620.
---------- VANCOUVER ----------
Dieterle, M.-E., Spinelli, S., Sadovskaya, I., Piuri, M., Cambillau, C. Evolved distal tail carbohydrate binding modules of Lactobacillus phage J-1: a novel type of anti-receptor widespread among lactic acid bacteria phages. Mol. Microbiol. 2017;104(4):608-620.