Escherichia coli tolQ Mutants Are Resistant to Filamentous Bacteriophages That Adsorb to the Tips, not the Shafts, of Conjugative Pili

Bradley, D. E.; Whelan, Jeanette

doi:10.1099/00221287-135-7-1857

Cited by 9 publications

(4 citation statements)

References 29 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…So far, TolA is the only protein that has shown direct interaction with the phage in the periplasm (9). In E. coli, the deletion of tolQ or tolR was reported to totally abolish Ff phage infection, similarly to a tolA mutant (7,8,10,53,54). However in V. cholerae, tolA deletion results in a CTX phage resistant strain, while tolQ or tolR can still be infected at low frequency (17).…”

Section: Mutantmentioning

confidence: 99%

Decoupling Filamentous Phage Uptake and Energy of the TolQRA Motor in Escherichia coli

et al. 2020

View full text Add to dashboard Cite

Filamentous phages are nonlytic viruses that specifically infect bacteria, establishing a persistent association with their host. The phage particle has no machinery for generating energy and parasitizes its host’s existing structures in order to cross the bacterial envelope and deliver its genetic material. The import of filamentous phages across the bacterial periplasmic space requires some of the components of a macrocomplex of the envelope known as the Tol system. This complex uses the energy provided by the proton motive force (pmf) of the inner membrane to perform essential and highly energy-consuming functions of the cell, such as envelope integrity maintenance and cell division. It has been suggested that phages take advantage of pmf-driven conformational changes in the Tol system to transit across the periplasm. However, this hypothesis has not been formally tested. In order to decouple the role of the Tol system in cell physiology and during phage parasitism, we used mutations on conserved essential residues known for inactivating pmf-dependent functions of the Tol system. We identified impaired Tol complexes that remain fully efficient for filamentous phage uptake. We further demonstrate that the TolQ-TolR homologous motor ExbB-ExbD, normally operating with the TonB protein, is able to promote phage infection along with full-length TolA. IMPORTANCE Filamentous phages are widely distributed symbionts of Gram-negative bacteria, with some of them being linked to genome evolution and virulence of their host. However, the precise mechanism that permits their uptake across the cell envelope is poorly understood. The canonical phage model Fd requires the TolQRA protein complex in the host envelope, which is suspected to translocate protons across the inner membrane. In this study, we show that phage uptake proceeds in the presence of the assembled but nonfunctional TolQRA complex. Moreover, our results unravel an alternative route for phage import that relies on the ExbB-ExbD proteins. This work provides new insights into the fundamental mechanisms of phage infection and might be generalized to other filamentous phages responsible for pathogen emergence.

show abstract

Section: Mutantmentioning

confidence: 99%

Decoupling Filamentous Phage Uptake and Energy of the TolQRA Motor in Escherichia coli

et al. 2020

View full text Add to dashboard Cite

show abstract

“…As mentioned above, certain host proteins participate in the injection process of phage fd DNA. The tolQ, toiR, and toU mutants of E. coli cannot be infected by phage fd and other phages which use the tips of conjugative pili as receptors (39,246). These mutants have a pleiotropic phenotype (for a review, see reference 319).…”

Section: Transmembrane Channels For the Translocationmentioning

confidence: 99%

Translocation of DNA across bacterial membranes.

Dreiseikelmann

1994

Microbiological Reviews

111

View full text Add to dashboard Cite

“…Images of individual virion STEM grids (Figure 3) appear to be wavier than images of most of the other viruses, although images of Inovirus species X are wavier than those of C2 (Bradley et al, 1981). C2 has an apparent persistance length that is much lower than those of the known class I Furthermore, C2 virus particles bind to the sides of the pili of the host cells, as does Pf3 (Bradley & Whelan, 1989), rather than at the ends, as is the case for Ff and Pfl (Caro & Schnoss, 1966;Bradley, 1973), or on the tapered sides of the tips, as is the case for tf-1 (Coetzee et al, 1987). Helical Protein Conformation.…”

Section: Discussionmentioning

confidence: 97%

C2, an Unusual Filamentous Bacterial Virus: Protein Sequence and Conformation, DNA Size and Conformation, and Nucleotide/Subunit Ratio

Kostrikis¹,

Reisberg²,

Kim³

et al. 1995

Biochemistry

View full text Add to dashboard Cite

Inovirus C2 is 1295 nm long and 6.8 nm in diameter, and its mass is 24 million Da. Its genome is a topologically circular, single-stranded DNA molecule of 8100 nucleotides. The DNA is packed in the virion as two antiparallel strands, with a rise per nucleotide in each strand of 3.2 A; it can be assigned spectroscopic properties like those of base-stacked, right-handed, double-stranded DNA. The stoichiometric ratio (n/s) of nucleotides to subunits of the major coat protein is close to 2. The protein subunit contains 52 amino acids, and the DNA sequence of its gene does not encode a signal peptide. The protein conformation in the virion is helical, mostly alpha-helix with perhaps some 3(10)-helix. The amino acid sequence of the DNA interaction domain of the subunit is unique among Inovirus species. On the basis of its coat protein sequence and available theories of helical symmetry in such structures, C2 appears to be either an unusual member of filamentous virus symmetry class II or the defining member of a new symmetry class.

show abstract

Escherichia coli tolQ Mutants Are Resistant to Filamentous Bacteriophages That Adsorb to the Tips, not the Shafts, of Conjugative Pili

Cited by 9 publications

References 29 publications

Decoupling Filamentous Phage Uptake and Energy of the TolQRA Motor in Escherichia coli

Decoupling Filamentous Phage Uptake and Energy of the TolQRA Motor in Escherichia coli

Translocation of DNA across bacterial membranes.

C2, an Unusual Filamentous Bacterial Virus: Protein Sequence and Conformation, DNA Size and Conformation, and Nucleotide/Subunit Ratio

Contact Info

Product

Resources

About