Actin Polymerization Drives Septation of Listeria monocytogenes namA Hydrolase Mutants, Demonstrating Host Correction of a Bacterial Defect
- 1 April 2011
- journal article
- Published by American Society for Microbiology in Infection and Immunity
- Vol. 79 (4), 1458-1470
- https://doi.org/10.1128/iai.01140-10
Abstract
The Gram-positive bacterial cell wall presents a structural barrier that requires modification for protein secretion and large-molecule transport as well as for bacterial growth and cell division. The Gram-positive bacterium Listeria monocytogenes adjusts cell wall architecture to promote its survival in diverse environments that include soil and the cytosol of mammalian cells. Here we provide evidence for the enzymatic flexibility of the murein hydrolase NamA and demonstrate that bacterial septation defects associated with a loss of NamA are functionally complemented by physical forces associated with actin polymerization within the host cell cytosol. L. monocytogenes Δ namA mutants formed long bacterial chains during exponential growth in broth culture; however, normal septation could be restored if mutant cells were cocultured with wild-type L. monocytogenes bacteria or by the addition of exogenous NamA. Surprisingly, Δ namA mutants were not significantly attenuated for virulence in mice despite the pronounced exponential growth septation defect. The physical force of L. monocytogenes -mediated actin polymerization within the cytosol was sufficient to sever Δ namA mutant intracellular chains and thereby enable the process of bacterial cell-to-cell spread so critical for L. monocytogenes virulence. The inhibition of actin polymerization by cytochalasin D resulted in extended intracellular bacterial chains for which septation was restored following drug removal. Thus, despite the requirement for NamA for the normal septation of exponentially growing L. monocytogenes cells, the hydrolase is essentially dispensable once L. monocytogenes gains access to the host cell cytosol. This phenomenon represents a notable example of eukaryotic host cell complementation of a bacterial defect.Keywords
This publication has 67 references indexed in Scilit:
- Listeria monocytogenes CtaP is a multifunctional cysteine transport‐associated protein required for bacterial pathogenesisMolecular Microbiology, 2009
- Listeria monocytogenes — from saprophyte to intracellular pathogenNature Reviews Microbiology, 2009
- The Posttranslocation Chaperone PrsA2 Contributes to Multiple Facets ofListeria monocytogenesPathogenesisInfection and Immunity, 2009
- Tools for Functional Postgenomic Analysis ofListeria monocytogenesApplied and Environmental Microbiology, 2008
- LysM, a widely distributed protein motif for binding to (peptido)glycansMolecular Microbiology, 2008
- Identification of NovelListeria monocytogenesSecreted Virulence Factors following Mutational Activation of the Central Virulence Regulator, PrfAInfection and Immunity, 2007
- Listeria monocytogenesSurface Proteins: from Genome Predictions to FunctionMicrobiology and Molecular Biology Reviews, 2007
- Identification of IspC, an 86-Kilodalton Protein Target of Humoral Immune Response to Infection with Listeria monocytogenes Serotype 4b, as a Novel Surface AutolysinJournal of Bacteriology, 2007
- The cell wall subproteome of Listeria monocytogenesProteomics, 2004
- ListeriaPathogenesis and Molecular Virulence DeterminantsClinical Microbiology Reviews, 2001