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EcoSal Plus

Domain 9: Life in Communities and the Environment

Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Denis Duché1, and Laetitia Houot2
  • Editors: Maria Sandkvist3, Eric Cascales4, Peter J. Christie5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Laboratoire d’Ingénierie des Systèmes Macromoléculaires, UMR7255, Institut de Microbiologie de la Méditerranée, Aix-Marseille Université—CNRS, 13402 Marseille, France; 2: Laboratoire d’Ingénierie des Systèmes Macromoléculaires, UMR7255, Institut de Microbiologie de la Méditerranée, Aix-Marseille Université— CNRS, 13402 Marseille, France; 3: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 4: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 5: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Received 07 September 2018 Accepted 16 November 2018 Published 25 January 2019
  • Address correspondence to Denis Duché, [email protected]; Laetitia Houot, [email protected]
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  • Abstract:

    Gram-negative bacteria have evolved a complex envelope to adapt and survive in a broad range of ecological niches. This physical barrier is the first line of defense against noxious compounds and viral particles called bacteriophages. Colicins are a family of bactericidal proteins produced by and toxic to and closely related bacteria. Filamentous phages have a complex structure, composed of at least five capsid proteins assembled in a long thread-shaped particle, that protects the viral DNA. Despite their difference in size and complexity, group A colicins and filamentous phages both parasitize multiprotein complexes of their sensitive host for entry. They first bind to a receptor located at the surface of the target bacteria before specifically recruiting components of the Tol system to cross the outer membrane and find their way through the periplasm. The Tol system is thought to use the proton motive force of the inner membrane to maintain outer membrane integrity during the life cycle of the cell. This review describes the sequential docking mechanisms of group A colicins and filamentous phages during their uptake by their bacterial host, with a specific focus on the translocation step, promoted by interactions with the Tol system.

  • Citation: Duché D, Houot L. 2019. Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0030-2018

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0030-2018
2019-01-25
2019-10-13

Abstract:

Gram-negative bacteria have evolved a complex envelope to adapt and survive in a broad range of ecological niches. This physical barrier is the first line of defense against noxious compounds and viral particles called bacteriophages. Colicins are a family of bactericidal proteins produced by and toxic to and closely related bacteria. Filamentous phages have a complex structure, composed of at least five capsid proteins assembled in a long thread-shaped particle, that protects the viral DNA. Despite their difference in size and complexity, group A colicins and filamentous phages both parasitize multiprotein complexes of their sensitive host for entry. They first bind to a receptor located at the surface of the target bacteria before specifically recruiting components of the Tol system to cross the outer membrane and find their way through the periplasm. The Tol system is thought to use the proton motive force of the inner membrane to maintain outer membrane integrity during the life cycle of the cell. This review describes the sequential docking mechanisms of group A colicins and filamentous phages during their uptake by their bacterial host, with a specific focus on the translocation step, promoted by interactions with the Tol system.

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Figures

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Figure 1

Schematic representation highlighting the similar general organization of colicin and phage pIII proteins for translocation (T or N1 domain), reception (R or N2 domain), and activity or anchoring (A or C domain). Structures of full-length colicin E3 (top left; PDB code 1JCH) bound to its immunity protein (in green), full-length colicin N (top right; PDB code 1A87), and M13 phage protein pIII-N1 and -N2 domains (bottom left; PDB code 1G3P) and superposition (bottom right) of TolAIII domain (gray) interacting with the colicin A T domain on its convex side (cocrystal; PDB code 3QDR) and interacting with G3P-N1 on its concave side (cocrystal PDB code 1TOL). The color code used for each protein domain is the same for panels A and B.

Citation: Duché D, Houot L. 2019. Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0030-2018
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Image of Figure 2
Figure 2

In stage 1, colicin binds to the OM receptor by its central domain ( 26 , 27 ). In stage 2(a), the disordered N-terminal segment of the T domain translocates through the OM β-barrel and interacts with a free periplasmic TolB or dissociates TolB from Pal ( 28 31 , 77 , 79 , 81 ). In stage 2(b), the N-terminal segment interacts with other Tol proteins ( 82 85 , 95 ). At this stage, the immunity protein of nuclease colicins is released ( 108 , 109 ). Then the unfolded C-terminal domain is thought to cross the OM through the interface between OmpF and the lipid bilayers ( 112 ) or directly through the OmpF porin ( 28 ). In stage 3, for pore-forming colicins () the C-terminal domain inserts spontaneously into the IM and forms voltage-gated channels that depolarize and kill the target bacteria (for a review, see reference 113 ). For nuclease colicins (), the C-terminal domain is cleaved by FtsH ( 114 , 115 ), an essential ATP-dependent IM protease, and spontaneously crosses the IM ( 116 ) or uses FtsH for its transfer ( 115 ). In stage 1, the phage minor coat protein pIII-N2 domain binds to the tip of an F pilus protruding from the cell surface ( 33 ). In stage 2, pilus retraction pulls the phage into the cell periplasm, possibly through the pilus secretin pore. Once there, the phage pIII-N1 domain interacts with the globular domain of TolA (TolAIII) ( 86 , 87 ). In , a direct interaction between TolAII and phage pIII-N2 has been reported (dashed arrow) ( 88 ). The PMF-dependent TolQR motor may trigger conformational changes of TolA that bring the phage particle in close contact with the IM. The phage uncapping process during the uptake stage (stage 3) is speculative. In the model, pIII oligomerizes to form a channel in the IM of the host through its C-ter domain (pIII-C). Then diffusion of the phage pVIII major coat protein in the IM leads to disassembly of the capsid, releasing the internal pressure of the structure. This force is thought to drive phage DNA injection through the IM pIII-C channel ( 102 , 103 ). The phage is composed of three to five copies of pIII, but only one copy has been represented, and other minor virion coat proteins have been omitted for simplicity. OM, outer membrane; IM, inner membrane; PG, peptidoglycan; peri, periplasm; cyto, cytoplasm; rec, receptor; trans, translocator.

Citation: Duché D, Houot L. 2019. Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0030-2018
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Tables

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Table 1

Host proteins required for reception and translocation of filamentous phages and group A colicins

Citation: Duché D, Houot L. 2019. Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0030-2018

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