Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120

Michel Plattner; Mikhail M. Shneider; Nikolay P. Arbatsky; Alexander S. Shashkov; Alexander O. Chizhov; Sergey Nazarov; Nikolai S. Prokhorov; Nicholas M.I. Taylor; Sergey A. Buth; Michela Gambino; Yilmaz Emre Gencay; Lone Brøndsted; Elizabeth M. Kutter; Yuriy A. Knirel; Petr G. Leiman

doi:10.1016/j.jmb.2019.07.022

Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120

Michel Plattner, Mikhail M. Shneider, Nikolay P. Arbatsky, Alexander S. Shashkov, Alexander O. Chizhov, Sergey Nazarov, Nikolai S. Prokhorov, Nicholas M.I. Taylor, Sergey A. Buth, Michela Gambino, Yilmaz Emre Gencay, Lone Brøndsted, Elizabeth M. Kutter, Yuriy A. Knirel, Petr G. Leiman^*

^*Corresponding author for this work

15 Citations (Scopus)

Abstract

Bacteriophages recognize their host cells with the help of tail fiber and tailspike proteins that bind, cleave, or modify certain structures on the cell surface. The spectrum of ligands to which the tail fibers and tailspikes can bind is the primary determinant of the host range. Bacteriophages with multiple tailspike/tail fibers are thought to have a wider host range than their less endowed relatives but the function of these proteins remains poorly understood. Here, we describe the structure, function, and substrate specificity of three tailspike proteins of bacteriophage CBA120—TSP2, TSP3 and TSP4 (orf211 through orf213, respectively). We show that tailspikes TSP2, TSP3 and TSP4 are hydrolases that digest the O157, O77, and O78 Escherichia coli O-antigens, respectively. We demonstrate that recognition of the E. coli O157:H7 host by CBA120 involves binding to and digesting the O157 O-antigen by TSP2. We report the crystal structure of TSP2 in complex with a repeating unit of the O157 O-antigen. We demonstrate that according to the specificity of its tailspikes TSP2, TSP3, and TSP4, CBA120 can infect E. coli O157, O77, and O78, respectively. We also show that CBA120 infects Salmonella enterica serovar Minnesota, and this host range expansion is likely due to the function of TSP1. Finally, we describe the assembly pathway and the architecture of the TSP1–TSP2–TSP3–TSP4 branched complex in CBA120 and its related ViI-like phages.

Original language	English
Journal	Journal of Molecular Biology
Volume	431
Issue number	19
Pages (from-to)	3718-3739
ISSN	0022-2836
DOIs	https://doi.org/10.1016/j.jmb.2019.07.022
Publication status	Published - 6 Sept 2019

Keywords

bacterial surface polysaccharides
bacteriophage attachment
host-cell recognition
NMR
x-ray crystallography

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10.1016/j.jmb.2019.07.022

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Plattner, M., Shneider, M. M., Arbatsky, N. P., Shashkov, A. S., Chizhov, A. O., Nazarov, S., Prokhorov, N. S., Taylor, N. M. I., Buth, S. A., Gambino, M., Gencay, Y. E., Brøndsted, L., Kutter, E. M., Knirel, Y. A., & Leiman, P. G. (2019). Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120. Journal of Molecular Biology, 431(19), 3718-3739. https://doi.org/10.1016/j.jmb.2019.07.022

Plattner, M, Shneider, MM, Arbatsky, NP, Shashkov, AS, Chizhov, AO, Nazarov, S, Prokhorov, NS, Taylor, NMI, Buth, SA, Gambino, M, Gencay, YE, Brøndsted, L, Kutter, EM, Knirel, YA & Leiman, PG 2019, 'Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120', Journal of Molecular Biology, vol. 431, no. 19, pp. 3718-3739. https://doi.org/10.1016/j.jmb.2019.07.022

@article{9e9a1dc3a1a94e1e95a1afcfd198d954,

title = "Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120",

abstract = "Bacteriophages recognize their host cells with the help of tail fiber and tailspike proteins that bind, cleave, or modify certain structures on the cell surface. The spectrum of ligands to which the tail fibers and tailspikes can bind is the primary determinant of the host range. Bacteriophages with multiple tailspike/tail fibers are thought to have a wider host range than their less endowed relatives but the function of these proteins remains poorly understood. Here, we describe the structure, function, and substrate specificity of three tailspike proteins of bacteriophage CBA120—TSP2, TSP3 and TSP4 (orf211 through orf213, respectively). We show that tailspikes TSP2, TSP3 and TSP4 are hydrolases that digest the O157, O77, and O78 Escherichia coli O-antigens, respectively. We demonstrate that recognition of the E. coli O157:H7 host by CBA120 involves binding to and digesting the O157 O-antigen by TSP2. We report the crystal structure of TSP2 in complex with a repeating unit of the O157 O-antigen. We demonstrate that according to the specificity of its tailspikes TSP2, TSP3, and TSP4, CBA120 can infect E. coli O157, O77, and O78, respectively. We also show that CBA120 infects Salmonella enterica serovar Minnesota, and this host range expansion is likely due to the function of TSP1. Finally, we describe the assembly pathway and the architecture of the TSP1–TSP2–TSP3–TSP4 branched complex in CBA120 and its related ViI-like phages.",

keywords = "bacterial surface polysaccharides, bacteriophage attachment, host-cell recognition, NMR, x-ray crystallography",

author = "Michel Plattner and Shneider, {Mikhail M.} and Arbatsky, {Nikolay P.} and Shashkov, {Alexander S.} and Chizhov, {Alexander O.} and Sergey Nazarov and Prokhorov, {Nikolai S.} and Taylor, {Nicholas M.I.} and Buth, {Sergey A.} and Michela Gambino and Gencay, {Yilmaz Emre} and Lone Br{\o}ndsted and Kutter, {Elizabeth M.} and Knirel, {Yuriy A.} and Leiman, {Petr G.}",

year = "2019",

month = sep,

day = "6",

doi = "10.1016/j.jmb.2019.07.022",

language = "English",

volume = "431",

pages = "3718--3739",

journal = "Journal of Molecular Biology",

issn = "0022-2836",

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number = "19",

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T1 - Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120

AU - Plattner, Michel

AU - Shneider, Mikhail M.

AU - Arbatsky, Nikolay P.

AU - Shashkov, Alexander S.

AU - Chizhov, Alexander O.

AU - Nazarov, Sergey

AU - Prokhorov, Nikolai S.

AU - Taylor, Nicholas M.I.

AU - Buth, Sergey A.

AU - Gambino, Michela

AU - Gencay, Yilmaz Emre

AU - Brøndsted, Lone

AU - Kutter, Elizabeth M.

AU - Knirel, Yuriy A.

AU - Leiman, Petr G.

PY - 2019/9/6

Y1 - 2019/9/6

N2 - Bacteriophages recognize their host cells with the help of tail fiber and tailspike proteins that bind, cleave, or modify certain structures on the cell surface. The spectrum of ligands to which the tail fibers and tailspikes can bind is the primary determinant of the host range. Bacteriophages with multiple tailspike/tail fibers are thought to have a wider host range than their less endowed relatives but the function of these proteins remains poorly understood. Here, we describe the structure, function, and substrate specificity of three tailspike proteins of bacteriophage CBA120—TSP2, TSP3 and TSP4 (orf211 through orf213, respectively). We show that tailspikes TSP2, TSP3 and TSP4 are hydrolases that digest the O157, O77, and O78 Escherichia coli O-antigens, respectively. We demonstrate that recognition of the E. coli O157:H7 host by CBA120 involves binding to and digesting the O157 O-antigen by TSP2. We report the crystal structure of TSP2 in complex with a repeating unit of the O157 O-antigen. We demonstrate that according to the specificity of its tailspikes TSP2, TSP3, and TSP4, CBA120 can infect E. coli O157, O77, and O78, respectively. We also show that CBA120 infects Salmonella enterica serovar Minnesota, and this host range expansion is likely due to the function of TSP1. Finally, we describe the assembly pathway and the architecture of the TSP1–TSP2–TSP3–TSP4 branched complex in CBA120 and its related ViI-like phages.

AB - Bacteriophages recognize their host cells with the help of tail fiber and tailspike proteins that bind, cleave, or modify certain structures on the cell surface. The spectrum of ligands to which the tail fibers and tailspikes can bind is the primary determinant of the host range. Bacteriophages with multiple tailspike/tail fibers are thought to have a wider host range than their less endowed relatives but the function of these proteins remains poorly understood. Here, we describe the structure, function, and substrate specificity of three tailspike proteins of bacteriophage CBA120—TSP2, TSP3 and TSP4 (orf211 through orf213, respectively). We show that tailspikes TSP2, TSP3 and TSP4 are hydrolases that digest the O157, O77, and O78 Escherichia coli O-antigens, respectively. We demonstrate that recognition of the E. coli O157:H7 host by CBA120 involves binding to and digesting the O157 O-antigen by TSP2. We report the crystal structure of TSP2 in complex with a repeating unit of the O157 O-antigen. We demonstrate that according to the specificity of its tailspikes TSP2, TSP3, and TSP4, CBA120 can infect E. coli O157, O77, and O78, respectively. We also show that CBA120 infects Salmonella enterica serovar Minnesota, and this host range expansion is likely due to the function of TSP1. Finally, we describe the assembly pathway and the architecture of the TSP1–TSP2–TSP3–TSP4 branched complex in CBA120 and its related ViI-like phages.

KW - bacterial surface polysaccharides

KW - bacteriophage attachment

KW - host-cell recognition

KW - NMR

KW - x-ray crystallography

U2 - 10.1016/j.jmb.2019.07.022

DO - 10.1016/j.jmb.2019.07.022

M3 - Journal article

C2 - 31325442

AN - SCOPUS:85069903638

SN - 0022-2836

VL - 431

SP - 3718

EP - 3739

JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

IS - 19

ER -

Structure and Function of the Branched Receptor-Binding Complex of Bacteriophage CBA120

Abstract

Keywords

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