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Title: Upregulation of peroxide scavenging enzymes and multidrug efflux proteins highlight an active sodium hypochlorite response in Pseudomonas fluorescens biofilms

Abstract

The oxidative biocide sodium hypochlorite is among the most commonly used antimicrobial agents in the control of surface-attached microbial communities (biofilms). Clarifying the genetic response of microorganisms in biofilms to hypochlorite may contribute to improved biofilm control strategies. Here, RNA-seq was used to investigate the differential gene expression response of industrially relevant Pseudomonas fluorescens biofilms to sub-lethal concentrations of sodium hypochlorite. Pseudomonas biofilms responded to hypochlorite exposure with increased transcription of genes encoding peroxide scavenging enzymes (e.g., alkyl hydroperoxide reductase (Ahp) and hydroperoxide resistance protein (Ohr)), oxidative stress repair enzymes (e.g., the periplasmic sulfoxide reductase YedYZ complex), and multidrug efflux (e.g., MexEF pumps). In addition, genes involved in amino acid synthesis and energy metabolism were down-regulated following hypochlorite exposure. This work improves the current understanding of genetic response mechanisms to biocides and contributes to the optimization of biocides and application strategies.

Authors:
 [1];  [2];  [3];  [4]
  1. National Energy Technology Lab. (NETL), Pittsburgh, PA (United States); Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States); Univ. of Pittsburgh, Pittsburgh, PA (United States). Dept. of Civil and Environmental Engineering
  2. U.S. Department of Agriculture, Clay Center, NE (United States). Agricultural Research Service, Roman L. Hruska US Meat Animal Research Center
  3. National Energy Technology Lab. (NETL), Pittsburgh, PA (United States)
  4. Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States); Univ. of Pittsburgh, Pittsburgh, PA (United States). Dept. of Civil and Environmental Engineering; Univ. of Notre Dame, South Bend, IN (United States). Dept. of Civil & Environmental Engineering & Earth Sciences
Publication Date:
Research Org.:
National Energy Technology Lab. (NETL), Pittsburgh, PA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1573910
Report Number(s):
NETL-PUB-22375
Journal ID: ISSN 0892-7014
Resource Type:
Accepted Manuscript
Journal Name:
Biofouling
Additional Journal Information:
Journal Volume: 35; Journal Issue: 3; Journal ID: ISSN 0892-7014
Publisher:
Taylor & Francis
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; hypochlorite; biofilm; transcriptome; RNA-seq

Citation Formats

Lipus, Daniel, Vikram, Amit, Gulliver, Djuna, and Bibby, Kyle. Upregulation of peroxide scavenging enzymes and multidrug efflux proteins highlight an active sodium hypochlorite response in Pseudomonas fluorescens biofilms. United States: N. p., 2019. Web. doi:10.1080/08927014.2019.1605357.
Lipus, Daniel, Vikram, Amit, Gulliver, Djuna, & Bibby, Kyle. Upregulation of peroxide scavenging enzymes and multidrug efflux proteins highlight an active sodium hypochlorite response in Pseudomonas fluorescens biofilms. United States. doi:10.1080/08927014.2019.1605357.
Lipus, Daniel, Vikram, Amit, Gulliver, Djuna, and Bibby, Kyle. Wed . "Upregulation of peroxide scavenging enzymes and multidrug efflux proteins highlight an active sodium hypochlorite response in Pseudomonas fluorescens biofilms". United States. doi:10.1080/08927014.2019.1605357.
@article{osti_1573910,
title = {Upregulation of peroxide scavenging enzymes and multidrug efflux proteins highlight an active sodium hypochlorite response in Pseudomonas fluorescens biofilms},
author = {Lipus, Daniel and Vikram, Amit and Gulliver, Djuna and Bibby, Kyle},
abstractNote = {The oxidative biocide sodium hypochlorite is among the most commonly used antimicrobial agents in the control of surface-attached microbial communities (biofilms). Clarifying the genetic response of microorganisms in biofilms to hypochlorite may contribute to improved biofilm control strategies. Here, RNA-seq was used to investigate the differential gene expression response of industrially relevant Pseudomonas fluorescens biofilms to sub-lethal concentrations of sodium hypochlorite. Pseudomonas biofilms responded to hypochlorite exposure with increased transcription of genes encoding peroxide scavenging enzymes (e.g., alkyl hydroperoxide reductase (Ahp) and hydroperoxide resistance protein (Ohr)), oxidative stress repair enzymes (e.g., the periplasmic sulfoxide reductase YedYZ complex), and multidrug efflux (e.g., MexEF pumps). In addition, genes involved in amino acid synthesis and energy metabolism were down-regulated following hypochlorite exposure. This work improves the current understanding of genetic response mechanisms to biocides and contributes to the optimization of biocides and application strategies.},
doi = {10.1080/08927014.2019.1605357},
journal = {Biofouling},
number = 3,
volume = 35,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
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    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
    • DOI: 10.1073/pnas.1424495112

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    journal, April 2011


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    journal, October 2011


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    journal, August 2014


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    journal, January 1992


    Differential expression in SAGE: accounting for normal between-library variation
    journal, August 2003


    Structural and functional characterization of the Pseudomonas hydroperoxide resistance protein Ohr
    journal, December 2002


    Microbial communities in Bakken region produced water
    journal, April 2018

    • Lipus, Daniel; Roy, Dhritikshama; Khan, Eakalak
    • FEMS Microbiology Letters, Vol. 365, Issue 12
    • DOI: 10.1093/femsle/fny107

    Physiological changes induced by the quaternary ammonium compound benzyldimethyldodecylammonium chloride on Pseudomonas fluorescens
    journal, February 2011

    • Ferreira, C.; Pereira, A. M.; Pereira, M. C.
    • Journal of Antimicrobial Chemotherapy, Vol. 66, Issue 5
    • DOI: 10.1093/jac/dkr028

    Role of bacterial efflux pumps in biofilm formation
    journal, February 2018

    • Alav, Ilyas; Sutton, J. Mark; Rahman, Khondaker Miraz
    • Journal of Antimicrobial Chemotherapy, Vol. 73, Issue 8
    • DOI: 10.1093/jac/dky042

    Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
    journal, September 1997

    • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
    • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
    • DOI: 10.1093/nar/25.17.3389

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    journal, August 2008


    Involvement of the oscA gene in the sulphur starvation response and in Cr(VI) resistance in Pseudomonas corrugata 28
    journal, January 2009


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    journal, December 2007


    LysM, a widely distributed protein motif for binding to (peptido)glycans
    journal, May 2008


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    journal, November 1996


    Tellurite: history, oxidative stress, and molecular mechanisms of resistance
    journal, July 2009


    Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress.
    journal, November 1996


    Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm
    journal, February 2002


    The roles of peroxide protective regulons in protecting Xanthomonas campestris pv. campestris from sodium hypochlorite stress
    journal, May 2015

    • Charoenlap, Nisanart; Sornchuer, Phornphan; Piwkam, Anong
    • Canadian Journal of Microbiology, Vol. 61, Issue 5
    • DOI: 10.1139/cjm-2014-0792

    RNA-seq analysis of single bovine blastocysts
    journal, January 2013


    Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
    journal, January 2009

    • Yamanaka, Takeshi; Furukawa, Tomoyo; Matsumoto-Mashimo, Chiho
    • BMC Microbiology, Vol. 9, Issue 1
    • DOI: 10.1186/1471-2180-9-11

    A scaling normalization method for differential expression analysis of RNA-seq data
    journal, March 2010


    Regulation of Organic Hydroperoxide Stress Response by Two OhrR Homologs in Pseudomonas aeruginosa
    journal, August 2016


    Effect of sodium hypochlorite on typical biofilms formed in drinking water distribution systems
    journal, February 2017

    • Lin, Huirong; Zhu, Xuan; Wang, Yuxin
    • Journal of Water and Health, Vol. 15, Issue 2
    • DOI: 10.2166/wh.2017.141

    The Oxidative Stress Agent Hypochlorite Stimulates c-di-GMP Synthesis and Biofilm Formation in Pseudomonas aeruginosa
    journal, November 2017


    Mechanisms of Actions of Sodium Hypochlorite in Cleaning and Disinfection Processes
    journal, January 2006