Periplasmic domains define holin-antiholin interactions in t4 lysis inhibition

J Bacteriol. 2005 Oct;187(19):6631-40. doi: 10.1128/JB.187.19.6631-6640.2005.

Abstract

Bacteriophage T4 effects host lysis with a holin, T, and an endolysin, E. T and E accumulate in the membrane and cytoplasm, respectively, throughout the period of late gene expression. At an allele-specific time, T triggers to disrupt the membrane, allowing E to enter the periplasm and attack the peptidoglycan. T triggering can be blocked by secondary infections, leading to the state of lysis inhibition (LIN). LIN requires the T4 antiholin, RI, and is sensitive to the addition of energy poisons. T is unusual among holins in having a large C-terminal periplasmic domain. The rI gene encodes a polypeptide of 97 residues, of which 72 are predicted to be a periplasmic domain. Here, we show that the periplasmic domain of RI is necessary and sufficient to block T-mediated lysis. Moreover, when overexpressed, the periplasmic domain of T (T(CTD)) was found to abolish LIN in T4 infections and to convert wild-type (wt) T4 plaques from small and fuzzy edged to the classic "r" large, sharp-edged plaque morphology. Although RI could be detected in whole cells, attempts to monitor it during subcellular fractionation were unsuccessful, presumably because RI is a highly unstable protein. However, fusing green fluorescence protein (GFP) to the N terminus of RI created a more stable chimera that could be demonstrated to form complexes with wild-type T(CTD) and also with its LIN-defective T75I variant. These results suggest that the function of the unusual periplasmic domain of T is to transduce environmental information for the real-time control of lysis timing.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Bacteriolysis / physiology*
  • Bacteriophage T4 / genetics*
  • Bacteriophage T4 / growth & development
  • Endopeptidases / chemistry
  • Endopeptidases / genetics
  • Endopeptidases / metabolism
  • Escherichia coli / virology*
  • Molecular Sequence Data
  • Periplasmic Proteins / chemistry
  • Periplasmic Proteins / genetics
  • Periplasmic Proteins / metabolism
  • Protein Structure, Tertiary
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Viral Proteins / chemistry
  • Viral Proteins / genetics*
  • Viral Proteins / metabolism*

Substances

  • Periplasmic Proteins
  • Recombinant Fusion Proteins
  • Viral Proteins
  • holin t protein, Enterobacteria phage T4
  • lysis protein T, bacteriophage T4
  • Endopeptidases
  • endolysin