Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells

Ricardo C. Guerrero-Ferreira, Mario Hupfeld, Sergey Nazarov, Nicholas M.I. Taylor, Mikhail M. Shneider, Jagan M. Obbineni, Martin J. Loessner, Takashi Ishikawa, Jochen Klumpp, Petr Leiman

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Contractile injection systems (bacteriophage tails, type VI secretions system, R-type pyocins, etc.) utilize a rigid tube/contractile sheath assembly for breaching the envelope of bacterial and eukaryotic cells. Among contractile injection systems, bacteriophages that infect Gram-positive bacteria represent the least understood members. Here, we describe the structure of Listeria bacteriophage A511 tail in its pre- and post-host attachment states (extended and contracted, respectively) using cryo-electron microscopy, cryo-electron tomography, and X-ray crystallography. We show that the structure of the tube-baseplate complex of A511 is similar to that of phage T4, but the A511 baseplate is decorated with different receptor-binding proteins, which undergo a large structural transformation upon host attachment and switch the symmetry of the baseplate-tail fiber assembly from threefold to sixfold. For the first time under native conditions, we show that contraction of the phage tail sheath assembly starts at the baseplate and propagates through the sheath in a domino-like motion.

Original languageEnglish (US)
Article numbere99455
JournalEMBO Journal
DOIs
StateAccepted/In press - Jan 1 2019

Fingerprint

Bacteriophages
Infection
Pyocins
Electron Microscope Tomography
Cryoelectron Microscopy
Bacteriophage T4
Listeria
Injections
X Ray Crystallography
Gram-Positive Bacteria
Eukaryotic Cells
X ray crystallography
Carrier Proteins
Electron microscopy
Tomography
Bacteria
Switches
Electrons
Fibers

Keywords

  • bacteriophage attachment
  • contractile injection system
  • cryo-electron microscopy
  • host cell recognition
  • X-ray crystallography

ASJC Scopus subject areas

  • Neuroscience(all)
  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

Guerrero-Ferreira, R. C., Hupfeld, M., Nazarov, S., Taylor, N. M. I., Shneider, M. M., Obbineni, J. M., ... Leiman, P. (Accepted/In press). Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells. EMBO Journal, [e99455]. https://doi.org/10.15252/embj.201899455

Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells. / Guerrero-Ferreira, Ricardo C.; Hupfeld, Mario; Nazarov, Sergey; Taylor, Nicholas M.I.; Shneider, Mikhail M.; Obbineni, Jagan M.; Loessner, Martin J.; Ishikawa, Takashi; Klumpp, Jochen; Leiman, Petr.

In: EMBO Journal, 01.01.2019.

Research output: Contribution to journalArticle

Guerrero-Ferreira, RC, Hupfeld, M, Nazarov, S, Taylor, NMI, Shneider, MM, Obbineni, JM, Loessner, MJ, Ishikawa, T, Klumpp, J & Leiman, P 2019, 'Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells', EMBO Journal. https://doi.org/10.15252/embj.201899455
Guerrero-Ferreira RC, Hupfeld M, Nazarov S, Taylor NMI, Shneider MM, Obbineni JM et al. Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells. EMBO Journal. 2019 Jan 1. e99455. https://doi.org/10.15252/embj.201899455
Guerrero-Ferreira, Ricardo C. ; Hupfeld, Mario ; Nazarov, Sergey ; Taylor, Nicholas M.I. ; Shneider, Mikhail M. ; Obbineni, Jagan M. ; Loessner, Martin J. ; Ishikawa, Takashi ; Klumpp, Jochen ; Leiman, Petr. / Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells. In: EMBO Journal. 2019.
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abstract = "Contractile injection systems (bacteriophage tails, type VI secretions system, R-type pyocins, etc.) utilize a rigid tube/contractile sheath assembly for breaching the envelope of bacterial and eukaryotic cells. Among contractile injection systems, bacteriophages that infect Gram-positive bacteria represent the least understood members. Here, we describe the structure of Listeria bacteriophage A511 tail in its pre- and post-host attachment states (extended and contracted, respectively) using cryo-electron microscopy, cryo-electron tomography, and X-ray crystallography. We show that the structure of the tube-baseplate complex of A511 is similar to that of phage T4, but the A511 baseplate is decorated with different receptor-binding proteins, which undergo a large structural transformation upon host attachment and switch the symmetry of the baseplate-tail fiber assembly from threefold to sixfold. For the first time under native conditions, we show that contraction of the phage tail sheath assembly starts at the baseplate and propagates through the sheath in a domino-like motion.",
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