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Title: Structural basis of superinfection exclusion by bacteriophage T4 Spackle

Abstract

A bacterial cell infected with T4 phage rapidly establishes resistance against further infections by the same or closely related T-even-type bacteriophages – a phenomenon called superinfection exclusion. Here we show that one of the T4 early gene products and a periplasmic protein, Spackle, forms a stoichiometric complex with the lysozyme domain of T4 tail spike protein gp5 and potently inhibits its activity. Crystal structure of the Spackle-gp5 lysozyme complex shows that Spackle binds to a horseshoe-shaped basic patch surrounding the oligosaccharide-binding cleft and induces an allosteric conformational change of the active site. In contrast, Spackle does not appreciably inhibit the lysozyme activity of cytoplasmic T4 endolysin responsible for cell lysis to release progeny phage particles at the final step of the lytic cycle. Our work reveals a unique mode of inhibition for lysozymes, a widespread class of enzymes in biology, and provides a mechanistic understanding of the T4 bacteriophage superinfection exclusion.

Authors:
 [1];  [1];  [1];  [1];  [2]; ORCiD logo [1]
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  1. Univ. of Minnesota, Minneapolis, MN (United States)
  2. Cornell Univ., Ithaca, NY (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division
Contributing Org.:
Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)
OSTI Identifier:
1729706
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Communications Biology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 1; Journal ID: ISSN 2399-3642
Publisher:
Springer Nature
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Shi, Ke, Oakland, Justin T., Kurniawan, Fredy, Moeller, Nicholas H., Banerjee, Surajit, and Aihara, Hideki. Structural basis of superinfection exclusion by bacteriophage T4 Spackle. United States: N. p., 2020. Web. doi:10.1038/s42003-020-01412-3.
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Shi, Ke, Oakland, Justin T., Kurniawan, Fredy, Moeller, Nicholas H., Banerjee, Surajit, & Aihara, Hideki. Structural basis of superinfection exclusion by bacteriophage T4 Spackle. United States. https://doi.org/10.1038/s42003-020-01412-3
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Shi, Ke, Oakland, Justin T., Kurniawan, Fredy, Moeller, Nicholas H., Banerjee, Surajit, and Aihara, Hideki. Thu . "Structural basis of superinfection exclusion by bacteriophage T4 Spackle". United States. https://doi.org/10.1038/s42003-020-01412-3. https://www.osti.gov/servlets/purl/1729706.
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@article{osti_1729706,
title = {Structural basis of superinfection exclusion by bacteriophage T4 Spackle},
author = {Shi, Ke and Oakland, Justin T. and Kurniawan, Fredy and Moeller, Nicholas H. and Banerjee, Surajit and Aihara, Hideki},
abstractNote = {A bacterial cell infected with T4 phage rapidly establishes resistance against further infections by the same or closely related T-even-type bacteriophages – a phenomenon called superinfection exclusion. Here we show that one of the T4 early gene products and a periplasmic protein, Spackle, forms a stoichiometric complex with the lysozyme domain of T4 tail spike protein gp5 and potently inhibits its activity. Crystal structure of the Spackle-gp5 lysozyme complex shows that Spackle binds to a horseshoe-shaped basic patch surrounding the oligosaccharide-binding cleft and induces an allosteric conformational change of the active site. In contrast, Spackle does not appreciably inhibit the lysozyme activity of cytoplasmic T4 endolysin responsible for cell lysis to release progeny phage particles at the final step of the lytic cycle. Our work reveals a unique mode of inhibition for lysozymes, a widespread class of enzymes in biology, and provides a mechanistic understanding of the T4 bacteriophage superinfection exclusion.},
doi = {10.1038/s42003-020-01412-3},
journal = {Communications Biology},
number = 1,
volume = 3,
place = {United States},
year = {2020},
month = {11}
}
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https://doi.org/10.1038/s42003-020-01412-3
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