Differences in Lactococcal Cell Wall Polysaccharide Structure Are Major Determining Factors in Bacteriophage Sensitivity

Typeset version

 

TY  - JOUR
  - Ainsworth, S,Sadovskaya, I,Vinogradov, E,Courtin, P,Guerardel, Y,Mahony, J,Grard, T,Cambillau, C,Chapot-Chartier, MP,van Sinderen, D
  - 2014
  - May
  - Mbio
  - Differences in Lactococcal Cell Wall Polysaccharide Structure Are Major Determining Factors in Bacteriophage Sensitivity
  - Validated
  - Altmetric: 3 ()
  - LACTIC-ACID BACTERIA ADSORPTION BLOCKING PLASMID RECEPTOR-BINDING PROTEIN PHAGE-HOST INTERACTIONS LYTIC BACTERIOPHAGE MODULAR STRUCTURE GENOME SEQUENCE GENE-EXPRESSION DNA-SEQUENCE TP901-1
  - 5
  - Analysis of the genetic locus encompassing a cell wall polysaccharide (CWPS) biosynthesis operon of eight strains of Lactococcus lactis, identified as belonging to the same CWPS type C genotype, revealed the presence of a variable region among the strains examined. The results allowed the identification of five subgroups of the C type named subtypes C-1 to C-5. This variable region contains genes encoding glycosyltransferases that display low or no sequence homology between the subgroups. In this study, we purified an acidic polysaccharide from the cell wall of L. lactis 3107 (subtype C-2) and confirmed that it is structurally different from the previously established CWPS of subtype C-1 L. lactis MG1363. The CWPS of L. lactis 3107 is composed of pentasaccharide repeating units linked by phosphodiester bonds with the structure 6-alpha-Glc-3-beta-Galf-3-beta-GlcNAc-2-beta-Galf-6-alpha-GlcNAc-1-P. Combinations of genes from the variable region of subtype C-2 were introduced into a mutant of subtype C-1 L. lactis NZ9000 deficient in CWPS biosynthesis. The resulting recombinant mutant synthesized a polysaccharide with a composition characteristic of that of subtype C-2 L. lactis 3107 and not wild-type C-1 L. lactis NZ9000. By challenging the recombinant mutant with various lactococcal phages, we demonstrated that CWPS is the host cell surface receptor of tested bacteriophages of both the P335 and 936 groups and that differences between the CWPS structures play a crucial role in determining phage host range.IMPORTANCE Despite the efforts of nearly 80 years of lactococcal phage research, the precise nature of the cell surface receptors of the P335 and 936 phage group receptors has remained elusive. This work demonstrates the molecular nature of a P335 group receptor while bolstering the evidence of its role in host recognition by phages of the 936 group and at least partially explains why such phages have a very narrow host range. The information generated will be instrumental in understanding the molecular mechanisms of how phages recognize specific saccharidic receptors located on the surface of their bacterial host.
  - 10.1128/mBio.00880-14
DA  - 2014/05
ER  - 
@article{V271354471,
   = {Ainsworth,  S and Sadovskaya,  I and Vinogradov,  E and Courtin,  P and Guerardel,  Y and Mahony,  J and Grard,  T and Cambillau,  C and Chapot-Chartier,  MP and van Sinderen,  D },
   = {2014},
   = {May},
   = {Mbio},
   = {Differences in Lactococcal Cell Wall Polysaccharide Structure Are Major Determining Factors in Bacteriophage Sensitivity},
   = {Validated},
   = {Altmetric: 3 ()},
   = {LACTIC-ACID BACTERIA ADSORPTION BLOCKING PLASMID RECEPTOR-BINDING PROTEIN PHAGE-HOST INTERACTIONS LYTIC BACTERIOPHAGE MODULAR STRUCTURE GENOME SEQUENCE GENE-EXPRESSION DNA-SEQUENCE TP901-1},
   = {5},
   = {{Analysis of the genetic locus encompassing a cell wall polysaccharide (CWPS) biosynthesis operon of eight strains of Lactococcus lactis, identified as belonging to the same CWPS type C genotype, revealed the presence of a variable region among the strains examined. The results allowed the identification of five subgroups of the C type named subtypes C-1 to C-5. This variable region contains genes encoding glycosyltransferases that display low or no sequence homology between the subgroups. In this study, we purified an acidic polysaccharide from the cell wall of L. lactis 3107 (subtype C-2) and confirmed that it is structurally different from the previously established CWPS of subtype C-1 L. lactis MG1363. The CWPS of L. lactis 3107 is composed of pentasaccharide repeating units linked by phosphodiester bonds with the structure 6-alpha-Glc-3-beta-Galf-3-beta-GlcNAc-2-beta-Galf-6-alpha-GlcNAc-1-P. Combinations of genes from the variable region of subtype C-2 were introduced into a mutant of subtype C-1 L. lactis NZ9000 deficient in CWPS biosynthesis. The resulting recombinant mutant synthesized a polysaccharide with a composition characteristic of that of subtype C-2 L. lactis 3107 and not wild-type C-1 L. lactis NZ9000. By challenging the recombinant mutant with various lactococcal phages, we demonstrated that CWPS is the host cell surface receptor of tested bacteriophages of both the P335 and 936 groups and that differences between the CWPS structures play a crucial role in determining phage host range.IMPORTANCE Despite the efforts of nearly 80 years of lactococcal phage research, the precise nature of the cell surface receptors of the P335 and 936 phage group receptors has remained elusive. This work demonstrates the molecular nature of a P335 group receptor while bolstering the evidence of its role in host recognition by phages of the 936 group and at least partially explains why such phages have a very narrow host range. The information generated will be instrumental in understanding the molecular mechanisms of how phages recognize specific saccharidic receptors located on the surface of their bacterial host.}},
   = {10.1128/mBio.00880-14},
  source = {IRIS}
}
AUTHORSAinsworth, S,Sadovskaya, I,Vinogradov, E,Courtin, P,Guerardel, Y,Mahony, J,Grard, T,Cambillau, C,Chapot-Chartier, MP,van Sinderen, D
YEAR2014
MONTHMay
JOURNAL_CODEMbio
TITLEDifferences in Lactococcal Cell Wall Polysaccharide Structure Are Major Determining Factors in Bacteriophage Sensitivity
STATUSValidated
TIMES_CITEDAltmetric: 3 ()
SEARCH_KEYWORDLACTIC-ACID BACTERIA ADSORPTION BLOCKING PLASMID RECEPTOR-BINDING PROTEIN PHAGE-HOST INTERACTIONS LYTIC BACTERIOPHAGE MODULAR STRUCTURE GENOME SEQUENCE GENE-EXPRESSION DNA-SEQUENCE TP901-1
VOLUME5
ISSUE
START_PAGE
END_PAGE
ABSTRACTAnalysis of the genetic locus encompassing a cell wall polysaccharide (CWPS) biosynthesis operon of eight strains of Lactococcus lactis, identified as belonging to the same CWPS type C genotype, revealed the presence of a variable region among the strains examined. The results allowed the identification of five subgroups of the C type named subtypes C-1 to C-5. This variable region contains genes encoding glycosyltransferases that display low or no sequence homology between the subgroups. In this study, we purified an acidic polysaccharide from the cell wall of L. lactis 3107 (subtype C-2) and confirmed that it is structurally different from the previously established CWPS of subtype C-1 L. lactis MG1363. The CWPS of L. lactis 3107 is composed of pentasaccharide repeating units linked by phosphodiester bonds with the structure 6-alpha-Glc-3-beta-Galf-3-beta-GlcNAc-2-beta-Galf-6-alpha-GlcNAc-1-P. Combinations of genes from the variable region of subtype C-2 were introduced into a mutant of subtype C-1 L. lactis NZ9000 deficient in CWPS biosynthesis. The resulting recombinant mutant synthesized a polysaccharide with a composition characteristic of that of subtype C-2 L. lactis 3107 and not wild-type C-1 L. lactis NZ9000. By challenging the recombinant mutant with various lactococcal phages, we demonstrated that CWPS is the host cell surface receptor of tested bacteriophages of both the P335 and 936 groups and that differences between the CWPS structures play a crucial role in determining phage host range.IMPORTANCE Despite the efforts of nearly 80 years of lactococcal phage research, the precise nature of the cell surface receptors of the P335 and 936 phage group receptors has remained elusive. This work demonstrates the molecular nature of a P335 group receptor while bolstering the evidence of its role in host recognition by phages of the 936 group and at least partially explains why such phages have a very narrow host range. The information generated will be instrumental in understanding the molecular mechanisms of how phages recognize specific saccharidic receptors located on the surface of their bacterial host.
PUBLISHER_LOCATION
ISBN_ISSN
EDITION
URL
DOI_LINK10.1128/mBio.00880-14
FUNDING_BODY
GRANT_DETAILS