Literature DB >> 27129969

Blue-Light Inhibition of Listeria monocytogenes Growth Is Mediated by Reactive Oxygen Species and Is Influenced by σB and the Blue-Light Sensor Lmo0799.

Beth O'Donoghue1, Kerrie NicAogáin1, Claire Bennett2, Alan Conneely2, Teresa Tiensuu3, Jörgen Johansson3, Conor O'Byrne4.   

Abstract

UNLABELLED: Listeria monocytogenes senses blue light via the flavin mononucleotide-containing sensory protein Lmo0799, leading to activation of the general stress response sigma factor SigB (σ(B)). In this study, we investigated the physiological response of this foodborne pathogen to blue light. We show that blue light (460 to 470 nm) doses of 1.5 to 2 mW cm(-2) cause inhibition of growth on agar-based and liquid culture media. The inhibitory effects are dependent on cell density, with reduced effects evident when high cell numbers are present. The addition of 20 mM dimethylthiourea, a scavenger of reactive oxygen species, or catalase to the medium reverses the inhibitory effects of blue light, suggesting that growth inhibition is mediated by the formation of reactive oxygen species. A mutant strain lacking σ(B) (ΔsigB) was found to be less inhibited by blue light than the wild type, likely indicating the energetic cost of deploying the general stress response. When a lethal dose of light (8 mW cm(-2)) was applied to cells, the ΔsigB mutant displayed a marked increase in sensitivity to light compared to the wild type. To investigate the role of the blue-light sensor Lmo0799, mutants were constructed that either had a deletion of the gene (Δlmo0799) or alteration in a conserved cysteine residue at position 56, which is predicted to play a pivotal role in the photocycle of the protein (lmo0799 C56A). Both mutants displayed phenotypes similar to the ΔsigB mutant in the presence of blue light, providing genetic evidence that residue 56 is critical for light sensing in L. monocytogenes Taken together, these results demonstrate that L. monocytogenes is inhibited by blue light in a manner that depends on reactive oxygen species, and they demonstrate clear light-dependent phenotypes associated with σ(B) and the blue-light sensor Lmo0799. IMPORTANCE: Listeria monocytogenes is a bacterial foodborne pathogen that can cause life-threatening infections in humans. It is known to be able to sense and respond to visible light. In this study, we examine the effects of blue light on the growth and survival of this pathogen. We show that growth can be inhibited at comparatively low doses of blue light, and that at higher doses, L. monocytogenes cells are killed. We present evidence suggesting that blue light inhibits this organism by causing the production of reactive oxygen species, such as hydrogen peroxide. We help clarify the mechanism of light sensing by constructing a "blind" version of the blue-light sensor protein. Finally, we show that activation of the general stress response by light has a negative effect on growth, probably because cellular resources are diverted into protective mechanisms rather than growth.
Copyright © 2016, American Society for Microbiology. All Rights Reserved.

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Year:  2016        PMID: 27129969      PMCID: PMC4907204          DOI: 10.1128/AEM.00685-16

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  48 in total

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Journal:  Genetics       Date:  2006-02-19       Impact factor: 4.562

2.  Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA.

Authors:  Andreas Möglich; Keith Moffat
Journal:  J Mol Biol       Date:  2007-08-02       Impact factor: 5.469

3.  In vivo mutational analysis of YtvA from Bacillus subtilis: mechanism of light activation of the general stress response.

Authors:  Marcela Avila-Pérez; Jocelyne Vreede; Yifen Tang; Onno Bende; Aba Losi; Wolfgang Gärtner; Klaas Hellingwerf
Journal:  J Biol Chem       Date:  2009-07-06       Impact factor: 5.157

4.  Analysis of the expression and function of the sigmaB-dependent general stress regulon of Bacillus subtilis during slow growth.

Authors:  T Schweder; A Kolyschkow; U Völker; M Hecker
Journal:  Arch Microbiol       Date:  1999 May-Jun       Impact factor: 2.552

5.  Photobiological activity of exogenous and endogenous porphyrin derivatives in Escherichia coli and Enterococcus hirae cells.

Authors:  F Gábor; K Szocs; P Maillard; G Csík
Journal:  Radiat Environ Biophys       Date:  2001-06       Impact factor: 1.925

6.  Photoinactivation of Acinetobacter baumannii and Escherichia coli B by a cationic hydrophilic porphyrin at various light wavelengths.

Authors:  Y Nitzan; H Ashkenazi
Journal:  Curr Microbiol       Date:  2001-06       Impact factor: 2.188

7.  Listeria monocytogenes sigma B regulates stress response and virulence functions.

Authors:  Mark J Kazmierczak; Sharon C Mithoe; Kathryn J Boor; Martin Wiedmann
Journal:  J Bacteriol       Date:  2003-10       Impact factor: 3.490

8.  RsbT and RsbV contribute to sigmaB-dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes.

Authors:  Soraya Chaturongakul; Kathryn J Boor
Journal:  Appl Environ Microbiol       Date:  2004-09       Impact factor: 4.792

9.  Molecular architecture of the "stressosome," a signal integration and transduction hub.

Authors:  Jon Marles-Wright; Tim Grant; Olivier Delumeau; Gijs van Duinen; Susan J Firbank; Peter J Lewis; James W Murray; Joseph A Newman; Maureen B Quin; Paul R Race; Alexis Rohou; Willem Tichelaar; Marin van Heel; Richard J Lewis
Journal:  Science       Date:  2008-10-03       Impact factor: 47.728

10.  Blue and red light modulates SigB-dependent gene transcription, swimming motility and invasiveness in Listeria monocytogenes.

Authors:  Nicolai Ondrusch; Jürgen Kreft
Journal:  PLoS One       Date:  2011-01-11       Impact factor: 3.240

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  22 in total

1.  The antimicrobial effect of blue light: What are behind?

Authors:  Tianhong Dai
Journal:  Virulence       Date:  2017-01-04       Impact factor: 5.882

2.  Regulation of the Erythrobacter litoralis DSM 8509 general stress response by visible light.

Authors:  Aretha Fiebig; Lydia M Varesio; Xiomarie Alejandro Navarreto; Sean Crosson
Journal:  Mol Microbiol       Date:  2019-06-07       Impact factor: 3.501

Review 3.  Antimicrobial blue light inactivation of pathogenic microbes: State of the art.

Authors:  Yucheng Wang; Ying Wang; Yuguang Wang; Clinton K Murray; Michael R Hamblin; David C Hooper; Tianhong Dai
Journal:  Drug Resist Updat       Date:  2017-10-13       Impact factor: 18.500

4.  The σB-dependent regulatory sRNA Rli47 represses isoleucine biosynthesis in Listeria monocytogenes through a direct interaction with the ilvA transcript.

Authors:  Catarina M Marinho; Patrícia T Dos Santos; Birgitte H Kallipolitis; Jörgen Johansson; Dmitriy Ignatov; Duarte N Guerreiro; Pascal Piveteau; Conor P O'Byrne
Journal:  RNA Biol       Date:  2019-06-26       Impact factor: 4.652

5.  In Vitro Evolution of Listeria monocytogenes Reveals Selective Pressure for Loss of SigB and AgrA Function at Different Incubation Temperatures.

Authors:  Duarte N Guerreiro; Jialun Wu; Emma McDermott; Dominique Garmyn; Peter Dockery; Aoife Boyd; Pascal Piveteau; Conor P O'Byrne
Journal:  Appl Environ Microbiol       Date:  2022-05-18       Impact factor: 5.005

6.  Molecular insights into intra-complex signal transmission during stressosome activation.

Authors:  Algirdas Miksys; Lifei Fu; M Gregor Madej; Duarte N Guerreiro; Susann Kaltwasser; Maria Conway; Sema Ejder; Astrid Bruckmann; Jon Marles-Wright; Richard J Lewis; Conor O'Byrne; Jan Pané-Farré; Christine Ziegler
Journal:  Commun Biol       Date:  2022-06-27

7.  Phylogenetic and Phenotypic Analyses of a Collection of Food and Clinical Listeria monocytogenes Isolates Reveal Loss of Function of Sigma B from Several Clonal Complexes.

Authors:  Jialun Wu; Kerrie NicAogáin; Olivia McAuliffe; Kieran Jordan; Conor O'Byrne
Journal:  Appl Environ Microbiol       Date:  2022-04-28       Impact factor: 5.005

8.  Mild Stress Conditions during Laboratory Culture Promote the Proliferation of Mutations That Negatively Affect Sigma B Activity in Listeria monocytogenes.

Authors:  Duarte N Guerreiro; Jialun Wu; Charlotte Dessaux; Ana H Oliveira; Teresa Tiensuu; Diana Gudynaite; Catarina M Marinho; Aoife Boyd; Francisco García-Del Portillo; Jörgen Johansson; Conor P O'Byrne
Journal:  J Bacteriol       Date:  2020-04-09       Impact factor: 3.490

9.  Exposure to Broad-Spectrum Visible Light Causes Major Transcriptomic Changes in Listeria monocytogenes EGDe.

Authors:  Kristin Sæbø Pettersen; Arvind Y M Sundaram; Taran Skjerdal; Yngvild Wasteson; Anne Kijewski; Toril Lindbäck; Marina Aspholm
Journal:  Appl Environ Microbiol       Date:  2019-10-30       Impact factor: 4.792

Review 10.  STAS Domain Only Proteins in Bacterial Gene Regulation.

Authors:  Brian E Moy; J Seshu
Journal:  Front Cell Infect Microbiol       Date:  2021-06-21       Impact factor: 5.293

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