DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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. https://doi.org/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. https://doi.org/10.1080/08927014.2019.1605357. https://www.osti.gov/servlets/purl/1573910.
@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 = {Wed May 08 00:00:00 EDT 2019},
month = {Wed May 08 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Impaired oxidative stress resistance of Bacillus subtilis sigB mutants and the role of katA and katE
journal, November 1996


Efficacy of common hospital biocides with biofilms of multi-drug resistant clinical isolates
journal, August 2008


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

Comparative Transcriptomic and Phenotypic Analysis of the Responses of Bacillus cereus to Various Disinfectant Treatments
journal, March 2010

  • Ceragioli, M.; Mols, M.; Moezelaar, R.
  • Applied and Environmental Microbiology, Vol. 76, Issue 10
  • DOI: 10.1128/AEM.03003-09

Global transcriptome analysis of the Mycobacterium bovis BCG response to sodium hypochlorite
journal, September 2009

  • Jang, Hyeung-Jin; Nde, Chantal; Toghrol, Freshteh
  • Applied Microbiology and Biotechnology, Vol. 85, Issue 1
  • DOI: 10.1007/s00253-009-2208-0

Ter-dependent stress response systems: novel pathways related to metal sensing, production of a nucleoside-like metabolite, and DNA-processing
journal, January 2012

  • Anantharaman, Vivek; Iyer, Lakshminarayan M.; Aravind, L.
  • Molecular BioSystems, Vol. 8, Issue 12
  • DOI: 10.1039/c2mb25239b

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


Biofilm formation and food safety in food industries
journal, September 2009


Structural details of the OxyR peroxide-sensing mechanism
journal, April 2015

  • Jo, Inseong; Chung, In-Young; Bae, Hee-Won
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
  • DOI: 10.1073/pnas.1424495112

Multidrug efflux pumps and resistance: regulation and evolution
journal, October 2003


Genome-Wide Transcriptional Responses of Escherichia coli K-12 to Continuous Osmotic and Heat Stresses
journal, March 2008

  • Gunasekera, T. S.; Csonka, L. N.; Paliy, O.
  • Journal of Bacteriology, Vol. 190, Issue 10
  • DOI: 10.1128/JB.01990-07

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


Response of Gram-positive bacteria to copper stress
journal, September 2009

  • Solioz, Marc; Abicht, Helge K.; Mermod, Mélanie
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 1
  • DOI: 10.1007/s00775-009-0588-3

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


Molecular Basis of Azithromycin-Resistant Pseudomonas aeruginosa Biofilms
journal, August 2005


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


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


Biofilm formation in food industries: A food safety concern
journal, June 2013


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


Toxicogenomic analysis of sodium hypochlorite antimicrobial mechanisms in Pseudomonas aeruginosa
journal, October 2006

  • Small, David A.; Chang, Wook; Toghrol, Freshteh
  • Applied Microbiology and Biotechnology, Vol. 74, Issue 1
  • DOI: 10.1007/s00253-006-0644-7

Oxidative stress, protein damage and repair in bacteria
journal, April 2017

  • Ezraty, Benjamin; Gennaris, Alexandra; Barras, Frédéric
  • Nature Reviews Microbiology, Vol. 15, Issue 7
  • DOI: 10.1038/nrmicro.2017.26

Molecular mechanism involved in the response to hydrogen peroxide stress in Acinetobacter oleivorans DR1
journal, August 2015

  • Kim, Jisun; Cho, Youjung; Jang, In-Ae
  • Applied Microbiology and Biotechnology, Vol. 99, Issue 24
  • DOI: 10.1007/s00253-015-6914-5

Biocides in Hydraulic Fracturing Fluids: A Critical Review of Their Usage, Mobility, Degradation, and Toxicity
journal, December 2014

  • Kahrilas, Genevieve A.; Blotevogel, Jens; Stewart, Philip S.
  • Environmental Science & Technology, Vol. 49, Issue 1
  • DOI: 10.1021/es503724k

Proteomics of the oxidative stress response induced by hydrogen peroxide and paraquat reveals a novel AhpC-like protein in Pseudomonas aeruginosa
journal, June 2011

  • Hare, Nathan J.; Scott, Nichollas E.; Shin, Eun Hye H.
  • PROTEOMICS, Vol. 11, Issue 15
  • DOI: 10.1002/pmic.201000807

Dynamics of the Action of Biocides in Pseudomonas aeruginosa Biofilms
journal, March 2011

  • Bridier, A.; Dubois-Brissonnet, F.; Greub, G.
  • Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 6
  • DOI: 10.1128/AAC.01760-10

Triclosan Can Select for an AdeIJK-Overexpressing Mutant of Acinetobacter baumannii ATCC 17978 That Displays Reduced Susceptibility to Multiple Antibiotics
journal, August 2014

  • Fernando, Dinesh M.; Xu, Wayne; Loewen, Peter C.
  • Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 11
  • DOI: 10.1128/AAC.03074-14

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

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


A dynamic and complex monochloramine stress response in Escherichia coli revealed by transcriptome analysis
journal, September 2013


Gene expression in Escherichia coli biofilms
journal, May 2004

  • Ren, D.; Bedzyk, L. A.; Thomas, S. M.
  • Applied Microbiology and Biotechnology, Vol. 64, Issue 4
  • DOI: 10.1007/s00253-003-1517-y

Metatranscriptome analysis of active microbial communities in produced water samples from the Marcellus Shale
journal, July 2016


Mapping and quantifying mammalian transcriptomes by RNA-Seq
journal, May 2008

  • Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth
  • Nature Methods, Vol. 5, Issue 7, p. 621-628
  • DOI: 10.1038/nmeth.1226

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


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

Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity.
journal, April 1996

  • Paulsen, I. T.; Brown, M. H.; Littlejohn, T. G.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 8
  • DOI: 10.1073/pnas.93.8.3630

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


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


Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes
journal, March 2006


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

Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
journal, December 2008

  • Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
  • Nature Protocols, Vol. 4, Issue 1
  • DOI: 10.1038/nprot.2008.211

Mechanisms of biofilm resistance to antimicrobial agents
journal, January 2001


Produced Water Exposure Alters Bacterial Response to Biocides
journal, October 2014

  • Vikram, Amit; Lipus, Daniel; Bibby, Kyle
  • Environmental Science & Technology, Vol. 48, Issue 21
  • DOI: 10.1021/es5036915

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


A critical assessment of the efficacy of biocides used during the hydraulic fracturing process in shale natural gas wells
journal, July 2012

  • Struchtemeyer, Christopher G.; Morrison, Michael D.; Elshahed, Mostafa S.
  • International Biodeterioration & Biodegradation, Vol. 71
  • DOI: 10.1016/j.ibiod.2012.01.013

Induction of Multidrug Resistance Mechanism in Escherichia coli Biofilms by Interplay between Tetracycline and Ampicillin Resistance Genes
journal, August 2009

  • May, T.; Ito, A.; Okabe, S.
  • Antimicrobial Agents and Chemotherapy, Vol. 53, Issue 11
  • DOI: 10.1128/AAC.00454-09

Bacterial transport of sulfate, molybdate, and related oxyanions
journal, February 2011

  • Aguilar-Barajas, Esther; Díaz-Pérez, César; Ramírez-Díaz, Martha I.
  • BioMetals, Vol. 24, Issue 4
  • DOI: 10.1007/s10534-011-9421-x

Bacterial adhesion and biofilms on surfaces
journal, September 2008

  • Garrett, Trevor Roger; Bhakoo, Manmohan; Zhang, Zhibing
  • Progress in Natural Science, Vol. 18, Issue 9
  • DOI: 10.1016/j.pnsc.2008.04.001

Biofilm formation in the industry: A review
journal, January 1992


Inactivation of Efflux Pumps Abolishes Bacterial Biofilm Formation
journal, October 2008

  • Kvist, M.; Hancock, V.; Klemm, P.
  • Applied and Environmental Microbiology, Vol. 74, Issue 23
  • DOI: 10.1128/AEM.01310-08

Comparative global transcription analysis of sodium hypochlorite, peracetic acid, and hydrogen peroxide on Pseudomonas aeruginosa
journal, July 2007

  • Small, David A.; Chang, Wook; Toghrol, Freshteh
  • Applied Microbiology and Biotechnology, Vol. 76, Issue 5
  • DOI: 10.1007/s00253-007-1072-z

Disinfection of bore well water with chlorine dioxide/sodium hypochlorite and hydrodynamic cavitation
journal, August 2014


The effects of glutaraldehyde on the control of single and dual biofilms of Bacillus cereus and Pseudomonas fluorescens
journal, April 2011


Characterization of MexE–MexF–OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa
journal, January 1997


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

Ketoglutarate Transport Protein KgtP Is Secreted through the Type III Secretion System and Contributes to Virulence in Xanthomonas oryzae pv. oryzae
journal, June 2012

  • Guo, Wei; Cai, Lu-Lu; Zou, Hua-Song
  • Applied and Environmental Microbiology, Vol. 78, Issue 16
  • DOI: 10.1128/AEM.07997-11

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 ECF sigma factor σ T is involved in osmotic and oxidative stress responses in Caulobacter crescentus
journal, December 2007


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


Resistance of bacterial biofilms to disinfectants: a review
journal, October 2011


Oxidative Stress Induction of the MexXY Multidrug Efflux Genes and Promotion of Aminoglycoside Resistance Development in Pseudomonas aeruginosa
journal, December 2010

  • Fraud, Sebastien; Poole, Keith
  • Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 3
  • DOI: 10.1128/AAC.01495-10

The ssu Locus Plays a Key Role in Organosulfur Metabolism in Pseudomonas putida S-313
journal, May 2000


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

Mechanism of action of sodium hypochlorite
journal, January 2002


Role of the Alkyl Hydroperoxide Reductase (ahpCF) Gene in Oxidative Stress Defense of the Obligate Anaerobe Bacteroides fragilis
journal, September 1999


Degradation of Staphylococcus aureus Biofilm Using Hydrolytic Enzymes Produced by Amazonian Endophytic Fungi
journal, March 2021

  • Matias, Rosiane Rodrigues; Sepúlveda, Ana Milena Gómez; Batista, Bárbara Nunes
  • Applied Biochemistry and Biotechnology, Vol. 193, Issue 7
  • DOI: 10.1007/s12010-021-03542-8

Response of gram-positive bacteria to copper stress
text, January 2010

  • Solioz, Marc; Abicht, Helge K.; Mermod, Mélanie
  • Springer-Verlag
  • DOI: 10.7892/boris.1743

Works referencing / citing this record:

Oxidative Stress Influences Pseudomonas aeruginosa Susceptibility to Antibiotics and Reduces Its Pathogenesis in Host
journal, January 2020