Chapter 30 : Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells

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Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells, Page 1 of 2

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The cell envelope of Gram-negative bacteria, such as , is characterized by the presence of two membranes, the inner (IM) and outer (OM) membranes, separated by the periplasm and a thin layer of peptidoglycan (PG). This envelope is a formidable barrier against a myriad of harmful compounds, while simultaneously allowing the entry of nutrients necessary for cell survival. However, this barrier, like the Maginot Line in France during the Second World War, is not completely impenetrable, and exogenous particles, including some toxins and viruses, can pierce it.

Citation: Duché D, Houot L. 2019. Similarities and Differences between Colicin and Filamentous Phage Uptake by Bacterial Cells, p 375-387. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0030-2018
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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, p 375-387. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. 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 ( ). 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 ( ). In stage 2(b), the N-terminal segment interacts with other Tol proteins ( ). At this stage, the immunity protein of nuclease colicins is released ( ). Then the unfolded C-terminal domain is thought to cross the OM through the interface between OmpF and the lipid bilayers ( ) or directly through the OmpF porin ( ). 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 ). For nuclease colicins (), the C-terminal domain is cleaved by FtsH ( ), an essential ATP-dependent IM protease, and spontaneously crosses the IM ( ) or uses FtsH for its transfer ( ). In stage 1, the phage minor coat protein pIII-N2 domain binds to the tip of an F pilus protruding from the cell surface ( ). 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) ( ). In , a direct interaction between TolAII and phage pIII-N2 has been reported (dashed arrow) ( ). 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 ( ). 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, p 375-387. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0030-2018
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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, p 375-387. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0030-2018

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