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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 32, 2016 - Issue 2
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Mini-review

Mini-review: Biofilm responses to oxidative stress

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Pages 167-178 | Received 27 Aug 2015, Accepted 14 Dec 2015, Published online: 27 Jan 2016

References

  • Amitai S, Yassin Y, Engelberg-Kulka H. 2004. MazF-mediated cell death in Escherichia coli: a point of no return. J Bacteriol. 186:8295–8300.10.1128/JB.186.24.8295-8300.2004
  • Anbar AD. 2008. Elements and evolution. Science. 322:1481–1483.10.1126/science.1163100
  • Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 55:373–399.10.1146/annurev.arplant.55.031903.141701
  • Arce Miranda JE, Sotomayor CE, Albesa I, Paraje MG. 2011. Oxidative and nitrosative stress in Staphylococcus aureus biofilm. FEMS Microbiol Lett. 315:23–29.10.1111/fml.2011.315.issue-1
  • Atack JM, Kelly DJ. 2009. Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol. 4:677–690.10.2217/fmb.09.44
  • Bai AJ, Rai VR. 2011. Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf. 10:184–194.
  • Bernier SP, Surette MG. 2013. Concentration-dependent activity of antibiotics in natural environments. Front Microbiol. 4:1–14.
  • Bjarnsholt T, Alhede M, Alhede M, Eickhardt-Sørensen SR, Moser C, Kuhl M, Jensen PO, Høiby N. 2013. The in vivo biofilm. Trends Microbiol. 21:466–474.10.1016/j.tim.2013.06.002
  • Bokare AD, Choi W. 2014. Review of iron-free Fenton-like systems for activating H2O2 in advanced oxidation processes. J Hazard Mat. 275:121–135.10.1016/j.jhazmat.2014.04.054
  • Boles BR, Singh PK. 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA. 105:12503–12508.10.1073/pnas.0801499105
  • Briviba K, Klotz LO, Sies H. 1997. Toxic and signaling effects of photochemically or chemically generated singletoxygenin biological systems. Biol Chem. 378:1259–1265.
  • Bruellhoff K, Fiedler J, Möller M, Groll J, Brenner RE. 2010. Surface coating strategies to prevent biofilm formation on implant surfaces. Int J Artif Organs. 33:646–653.
  • Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Intern Microbiol. 3:3–8.
  • Calabrese V, Cornelius C, Cuzzocrea S, Iavicoli I, Rizzarelli E, Calabrese EJ. 2011. Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity. Molec Aspects Med. 32:279–304.10.1016/j.mam.2011.10.007
  • Cáp M, Váchová L, Palková Z. 2012. Reactive oxygen species in the signaling and adaptation of multicellular microbial communities. Oxid Med Cell Longev: 976753.
  • Cappitelli F, Polo A, Villa F. 2014. Biofilm formation in food processing environments is still poorly understood and controlled. Food Engineer Rev. 6:29–42.10.1007/s12393-014-9077-8
  • Cappitelli F, Principi P, Sorlini C. 2006. Biodeterioration of modern materials in contemporary collections: can biotechnology help? Trends Biotechnol. 24:350–354.10.1016/j.tibtech.2006.06.001
  • Cattò C, Dell’Orto S, Villa F, Villa S, Gelain A, Vitali A, Marzano V, Baroni S, Forlani F, Cappitelli F. 2015. Unravelling the structural and molecular basis responsible for the anti-biofilm activity of zosteric acid. PloS One. 10:e0131519.10.1371/journal.pone.0131519
  • Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. 2008. The biology and future prospects of antivirulence therapies. Nat Rev Microbiol. 6:17–27.10.1038/nrmicro1818
  • Chattopadhyay MK, Raghu G, Sharma YV, Biju AR, Rajasekharan MV, Shivaji S. 2011. Increase in oxidative stress at low temperature in an antarctic bacterium. Curr Microbiol. 62:544–546.10.1007/s00284-010-9742-y
  • Chen J, Shen J, Solem C, Jensen PR. 2013. Oxidative stress at high temperatures in Lactococcus lactis due to an insufficient supply of riboflavin. Appl Environ Microbiol. 79:6140–6147.10.1128/AEM.01953-13
  • Chutoam P, Charoensawan V, Wongtrakoongate P, Kumarth A, Buphamalai P, Tungpradabkul S. 2013. RpoS and oxidative stress conditions regulate succinyl-CoA: 3-ketoacid-coenzyme A transferase (SCOT) expression in Burkholderia pseudomallei. Microbiol Immunol. 57:605–615.
  • Clare AS. 1996. Marine natural product antifoulants: status and potential. Biofouling. 9:211–229.10.1080/08927019609378304
  • Clare AS, Rittschof D, Gerhart D, Maki J. 1992. Molecular approaches to nontoxic antifouling. Invertebr Reprod Dev. 22:67–76.10.1080/07924259.1992.9672258
  • Collet A, Cosette P, Beloin C, Ghigo JM, Rihouey C, Lerouge P, Junter GA, Jouenne T. 2008. Impact of rpoS deletion on the proteome of Escherichia coli grown planktonically and as biofilm. J Proteome Res. 7:4659–4669.10.1021/pr8001723
  • Conlin PL, Chandler JR, Kerr B. 2014. Games of life and death: antibiotic resistance and production through the lens of evolutionary game theory. Curr Opin Microbiol. 21:35–44.10.1016/j.mib.2014.09.004
  • Cornelis P, Dingemans J. 2013. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol. 3:1–7.
  • Corona-Izquierdo FP, Membrillo-Hernández J. 2002. A mutation in rpoS enhances biofilm formation in Escherichia coli during exponential phase of growth. FEMS Microbiol Lett. 211:105–110.10.1111/fml.2002.211.issue-1
  • Costerton JW, Cheng KJ, Geesy GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ. 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol. 41:435–464.10.1146/annurev.mi.41.100187.002251
  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu Rev Microbiol. 49:711–45.
  • Danese PN, Pratt L, Dove SL, Kolter R. 2000. The outer membrane protein, Antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol. 37:424–432.10.1046/j.1365-2958.2000.02008.x
  • Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S. 2013. Marine bacteria: potential candidates for enhanced bioremediation. Appl Microb Biotechnol. 97:561–571.10.1007/s00253-012-4584-0
  • Davey ME, O’Toole G. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev. 64:847–867.10.1128/MMBR.64.4.847-867.2000
  • Davidson JF, Whyte B, Bissinger PH, Schiestl RH. 1996. Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 93:5116–5121.10.1073/pnas.93.10.5116
  • DePas WH, Hufnagel D, Lee JS, Blanco LP, Bernstein HC, Fisher ST, James GA, Stewart PS, Chapman MR. 2013. Iron induces bimodal population development by Escherichia coli. Proc Natl Acad Sci USA. 110:2629–2634.10.1073/pnas.1218703110
  • Dietrich LEP, Teal TK, Price-Whelan A, Newman DK. 2008. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science. 321:1203–1206.10.1126/science.1160619
  • Dorsey-Oresto A, Lu T, Mosel M, Wang X, Salz T, Drlica K, Zhao X. 2013. YihE Kinase is a central regulator of programmed cell death in bacteria. Cell Reports. 3:528–537.10.1016/j.celrep.2013.01.026
  • Drago L. 2009. Bacteria and biofilm in respiratory tract infections. Infect Med. 17:3–9.
  • Dwyer DJ, Belenky PA, Yang JH, MacDonald IC, Martell JD, Takahashi N, Chan CT, Lobritz MA, Braff D, Schwarz EG, et al. 2014. Antibiotics induce redox-related physiological alterations as part of their lethality. Proc Natl Acad Sci USA. 111:E2100–E2109.10.1073/pnas.1401876111
  • Dwyer DJ, Collins JJ, Walker GC. 2015. Unraveling the physiological complexities of antibiotic lethality. Annu Rev Pharmacol Toxicol. 55:313–332.10.1146/annurev-pharmtox-010814-124712
  • Ezraty B, Vergnes A, Banzhaf M, Duverger Y, Huguenot A, Brochado AR, Su SY, Espinosa L, Loiseau L, Py B, Barras F. 2013. Fe-S cluster biosynthesis controls uptake of aminoglycosides in a ROS-less death pathway. Science. 340:1583–1587.10.1126/science.1238328
  • Fester T, Hause G. 2005. Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza. 15:373–379.10.1007/s00572-005-0363-4
  • Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science. 336:315–319.10.1126/science.1219192
  • Gambino M, Marzano V, Villa F, Vitali A, Vannini C, Landini P, Cappitelli F. 2015. Effects of sub-lethal doses of silver nanoparticles on Bacillus subtilis planktonic and sessile cells. J Appl Microbiol. 118:1103–1115.10.1111/jam.2015.118.issue-5
  • García-Contreras R, Nuñez-López L, Jasso-Chávez R, Kwan BW, Belmont J, Rangel-Vega A, Belmont JA, Rangel-Vega A, Maeda T, Wood TK. 2015. Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J. 9:115–125.10.1038/ismej.2014.98
  • Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M. 2001. The phagosome proteome: insight into phagosome functions. J Cell Biol. 152:165–180.10.1083/jcb.152.1.165
  • Gerschman R, Gilbert DL, Nye SW, Dwyer P, Fenn WO. 1954. Oxygen poisoning and X-irradiation: a mechanism in common. Science. 119:623–626.10.1126/science.119.3097.623
  • Gilbert P, Mc Bain AJ. 2003. Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin Microbiol Rev. 16:189–208.10.1128/CMR.16.2.189-208.2003
  • Green J, Paget MS. 2004. Bacterial redox sensors. Nat Rev Microbiol. 2:954–966.10.1038/nrmicro1022
  • Guerrero R, Margulis L, Berlanga M. 2013. Symbiogenesis: the holobiont as a unit of evolution. Int Microbiol. 16:133–143.
  • Hadfield MG. 2011. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Ann Rev Mar Sci. 3:453–470.10.1146/annurev-marine-120709-142753
  • Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2:95–108.10.1038/nrmicro821
  • Hassett DJ, Ma JS, Elkins JG, McDermott T, Ochsner UA, West SE, Huang CT, Fredericks J, Burnett S, Stewart PS, et al. 1999. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol. 34:1082–1093.10.1046/j.1365-2958.1999.01672.x
  • Hay ID, Wang Y, Moradali MF, Rehman ZU, Rehm BH. 2014. Genetics and regulation of bacterial alginate production. Environ Microbiol. 16:2997–3011.10.1111/emi.2014.16.issue-10
  • Hengge-Aronis R. 1999. Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr Opin Microbiol. 2:148–152.10.1016/S1369-5274(99)80026-5
  • Honma K, Mishima E, Inagaki S, Sharma A. 2009. The OxyR homologue in Tannerella forsythia regulates expression of oxidative stress responses and biofilm formation. Microbiology. 155:1912–1922.10.1099/mic.0.027920-0
  • Huang CJ, Wang ZC, Huang HY, Huang HD, Peng HL. 2013. YjcC, a c-di-GMP phosphodiesterase protein, regulates the oxidative stress response and virulence of Klebsiella pneumoniae CG43. PloS One. 8:e66740.10.1371/journal.pone.0066740
  • Imlay J. 2003. Pathways of oxidative damage. Annu Rev Microbiol. 57:395–418.10.1146/annurev.micro.57.030502.090938
  • Imlay J. 2013. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol. 11:443–454.10.1038/nrmicro3032
  • Imlay J. 2015. Diagnosing oxidative stress in bacteria: not as easy as you might think. Curr Opin Microbiol. 24:124–131.10.1016/j.mib.2015.01.004
  • Jamet A, Siguad S, Van de Sype G, Puppo A, Herouart D. 2003. Expression of the bacterial catalase genes during Sinorhizobium meliloti- Medicago sativa symbiosis and their crucial role during the infection process. Mol Plant Microbe Interact. 16:217–225.10.1094/MPMI.2003.16.3.217
  • Kang YS, Lee Y, Jung H, Jeon CO, Madsen EL, Park W. 2007. Overexpressing antioxidant enzymes enhances naphthalene biodegradation in Pseudomonas sp. strain As1. Microbiology. 153:3246–3254.10.1099/mic.0.2007/008896-0
  • Keren I, Wu Y, Inocencio J, Mulcahy LR, Lewis K. 2013. Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science. 339:1213–1216.10.1126/science.1232688
  • Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell. 130:797–810.10.1016/j.cell.2007.06.049
  • Landini P. 2009. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Res Microbiol. 160:259–266.10.1016/j.resmic.2009.03.001
  • Lewis K. 2008. Multidrug tolerance of biofilms and persister cells. Curr Topics Microbiol Immunol. 322:107–131.
  • Ligeza A, Tikhonov AN, Hyde JS, Subczynski WK. 1998. Oxygen permeability of thylakoid membranes: electron paramagnetic resonance spin labeling study. Biochim Biophys Acta. 1365:453–463.10.1016/S0005-2728(98)00098-X
  • Linley E, Denyer SP, McDonnell G, Simons C, Maillard JY. 2012. Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action. J Antimicrob Chemother. 67:1589–1596.10.1093/jac/dks129
  • Loprasert S, Sallabhan R, Whangsuk W, Mongkolsuk S. 2000. Characterization and mutagenesis of fur gene from Burkholderia pseudomallei. Gene. 254:129–137.10.1016/S0378-1119(00)00279-1
  • Loprasert S, Whangsuk W, Sallabhan R, Mongkolsuk S. 2004. DpsA protects the human pathogen Burkholderia pseudomallei against organic hydroperoxide. Arch Microbiol. 182:96–101.10.1007/s00203-004-0694-0
  • Lucas-Elío P, Goodwin L, Woyke T, Pitluck S, Nolan M, Kyrpides NC, Detter JC, Copeland A, Teshima H, Bruce D, et al. 2012. Complete genome sequence of the melanogenic marine bacterium Marinomonas mediterranea type strain (MMB-1(T)). Stand Genomic Sci. 6:63–73.10.4056/sigs.2545743
  • Lumjiaktase P, Diggle SP, Loprasert S, Tungpradabkul S, Daykin M, Cámara M, Williams P, Kunakorn M. 2006. Quorum sensing regulates dpsA and the oxidative stress response in Burkholderia pseudomallei. Microbiology. 152:3651–3659.10.1099/mic.0.29226-0
  • Lushchak VI. 2014. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact. 224:164–175.10.1016/j.cbi.2014.10.016
  • Maddula VS, Zhang Z, Pierson EA, Pierson LS. 2006. Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30-84. Microb Ecol. 52:289–301.10.1007/s00248-006-9064-6
  • Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature. 426:306–310.10.1038/nature02122
  • Marathe SA, Kumar R, Ajitkumar P, Nagaraja V, Chakravortty D. 2013. Curcumin reduces the antimicrobial activity of ciprofloxacin against Salmonella typhimurium and Salmonella typhi. J Antimicrob Chemother. 68:139–152.10.1093/jac/dks375
  • Martinez JL. 2009. The role of natural environments in the evolution of resistance traits in pathogenic bacteria. Proc Biol Sci. 276:2521–2530.10.1098/rspb.2009.0320
  • Martinez A, Kolter R. 1997. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol. 179:5188–5194.
  • Matallana-Surget S, Joux F, Raftery MJ, Cavicchioli R. 2009. The response of the marine bacterium Sphingopyxis alaskensis to solar radiation assessed by quantitative proteomics. Environ Microbiol. 11:2660–2675.10.1111/emi.2009.11.issue-10
  • Mathee K, Ciofu O, Sternberg C, Lindum PW, Campbell JI. 1999. Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology. 145:1349–1357.10.1099/13500872-145-6-1349
  • Mavrodi DV, Peever TL, Mavrodi OV, Parejko J, Raaijmakers JM, Lemanceau P, Mazurier S, Heide L, Blankenfeldt W, Weller DW, Thomashow LS. 2010. Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol. 76:866–879.10.1128/AEM.02009-09
  • Mc Cay PH, Ocampo-Sosa AA, Fleming GT. 2010. Effect of subinhibitory concentrations of benzalkonium chloride on the competitiveness of Pseudomonas aeruginosa grown in continuous culture. Microbiology. 156:30–38.10.1099/mic.0.029751-0
  • Mc Dougald D, Rice S, Barraud N, Steinberg PD, Kjelleberg S. 2011. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol. 10:39–50.
  • Méndez-Ortiz MM, Hyodo M, Hayakawa Y, Membrillo-Hernández J. 2006. Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3′,5′-cyclic diguanylic acid. J Biol Chem. 281:8090–8099.10.1074/jbc.M510701200
  • Milferstedt K, Santa-Catalina G, Godon JJ, Escudié R, Bernet N. 2013. Disturbance frequency determines morphology and community development in multi-species biofilm at the landscape scale. PLoS One. 8:1–14.
  • Mirzajani F, Askari H, Hamzelou S, Farzaneh M, Ghassempour A. 2013. Effect of silver nanoparticles on Oryza sativa L. and its rhizosphere bacteria. Ecotoxicol Environ Saf. 88:48–54.10.1016/j.ecoenv.2012.10.018
  • Molina-Quintero LR, Lucas-Elío P, Sanchez-Amat A. 2010. Regulation of the Marinomonas merditerranea antimicrobial protein lysine oxidase by L-lysine and the sensor histidine kinase PpoS. Appl Environ Microbiol. 76:6141–6149.10.1128/AEM.00690-10
  • Monds RD, O’Toole G. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17:73–87.10.1016/j.tim.2008.11.001
  • Morgan R, Kohn S, Hwang SH, Hassett DJ, Sauer K. 2006. BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol. 188:7335–7343.10.1128/JB.00599-06
  • Murata M, Fujimoto H, Nishimura K, Charoensuk K, Nagamitsu H, Raina S, Kosaka T, Oshima T, Ogasawara N, Yamada M. 2011. Molecular strategy for survival at a critical high temperature in Escherichia coli. PLoS One. 6:e0020063.
  • Nanda AK, Andrio E, Marino D, Pauly N, Dunand C. 2010. Reactive oxygen species during plant-microorganism early interactions. J Integrative Plant Biol. 52:195–204.10.1111/jipb.2010.52.issue-2
  • Nicolella C. 2000. Wastewater treatment with particulate biofilm reactors. J Biotechnol. 80:1–33.10.1016/S0168-1656(00)00229-7
  • Oh E, Jeon B. 2014. Role of alkyl hydroperoxide reductase (AhpC) in the biofilm formation of Campylobacter jejuni. PLoS One. 9:e87312.10.1371/journal.pone.0087312
  • Ortiz de Orué Lucana D, Wedderhoff I, Groves MR. 2012. ROS-mediated signalling in bacteria: zinc-containing Cys-X-X-Cys redox centres and iron-based oxidative stress. J Signal Transd. 2012:1–9.
  • Pacher P, Beckman JS, Liaudet L. 2007. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 87:315–424.10.1152/physrev.00029.2006
  • Painter KL, Strange E, Parkhill J, Bamford KB, Armstrong-James D, Edwards AM. 2015. Staphylococcus aureus adapts to oxidative stress by producing H2O2-resistant small colony variants via the SOS response. Infection Immun. 83:1830–1844.10.1128/IAI.03016-14
  • Pan Y. 2011. Mitochondria, reactive oxygen species, and chronological aging: a message from yeast. Experim Gerontol. 46:847–852.10.1016/j.exger.2011.08.007
  • Patten CL, Kirchhof MG, Schertzberg MR, Morton R, Schellhorn HE. 2004. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics. 272:580–591.10.1007/s00438-004-1089-2
  • Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V. 2013. Endogenous stress caused by faulty oxidation reactions fosters evolution of 2, 4-dinitrotoluene-degrading bacteria. PLoS Genetics. 9:e1003764.10.1371/journal.pgen.1003764
  • Pierson LS, Pierson EA. 2010. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol. 86:1659–1670.10.1007/s00253-010-2509-3
  • Pogliano J, Lynch AS, Belin D, Lin EC, Beckwith J. 1997. Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev. 11:1169–1182.10.1101/gad.11.9.1169
  • Polo A, Diamanti MV, Bjarnsholt T, Høiby N, Villa F, Pedeferri MP, Cappitelli F. 2011. Effects of photoactivated titanium dioxide nanopowders and coating on planktonic and biofilm growth of Pseudomonas aeruginosa. Photochem Photobiol. 87:1387–1394.10.1111/php.2011.87.issue-6
  • Polo A, Foladori P, Ponti B, Bettinetti R, Gambino M, Villa F, Cappitelli F. 2014. Evaluation of zosteric acid for mitigating biofilm formation of Pseudomonas putida isolated from a membrane bioreactor system. Int J Mol Sci. 15:9497–9518.10.3390/ijms15069497
  • Price-Whelan A, Dietrich LE, Newman DK. 2006. Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol. 2:71–78.10.1038/nchembio764
  • Qin Q-L, Li Y, Zhang Y-J, Zhou Z-M, Zhang W-X, Chen X-L, Zhang X-Y, Zhou B-C, Wang L, Zhang Y-Z. 2011. Comparative genomics reveals a deep-sea sediment-adapted life style of Pseudoalteromonas sp. SM9913. ISME J. 5:274–284.10.1038/ismej.2010.103
  • Raivio TL, Silhavy TJ. 2001. Periplasmic stress and ECF sigma factors. Annu Rev Microbiol. 55:591–624.10.1146/annurev.micro.55.1.591
  • Rice S, Tan CH, Mikkelsen PJ, Kung V, Tay M, Hauser A, McDougald D, Webb JS, Kjelleberg S. 2009. The biofilm life-cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J. 3:271–282.10.1038/ismej.2008.109
  • Rinaudi LV, Giordano W. 2010. An integrated view of biofilm formation in rhizobia. FEMS Microbiol Lett. 304:1–11.10.1111/fml.2010.304.issue-1
  • Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M. 2004. Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Mol Plant Microbe Interact. 17:1294–1305.10.1094/MPMI.2004.17.12.1294
  • Rudrappa T, Biedrzycki ML, Bais HP. 2008. Causes and consequences of plant-associated biofilms. FEMS Microbiol Ecol. 64:153–166.10.1111/fem.2008.64.issue-2
  • Ryder VJ, Chopra I, O’Neill AJ. 2012. Increased mutability of staphylococci in biofilms as a consequence of oxidative stress. PLoS One. 7:e47695.10.1371/journal.pone.0047695
  • Saint-Ruf C, Garfa-Traoré M, Collin V, Cordier C, Franceschi C, Matic I. 2014. Massive diversification in aging colonies of Escherichia coli. J Bacteriol. 196:3059–3073.10.1128/JB.01421-13
  • Schellhorn HE, Stones VL. 1992. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol. 174:4769–4776.
  • Schembri M, Kjaergaard K, Klemm P. 2003. Global gene expression in Escherichia coli biofilms. Mol Microbiol. 48:253–267.10.1046/j.1365-2958.2003.03432.x
  • Seaver LC, Imlay JA. 2004. Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem. 279:48742–48750.10.1074/jbc.M408754200
  • Seib KL, Wu HJ, Srikhanta YN, Edwards JL, Falsetta ML, Hamilton AJ, Maguire TL, Grimmond SM, Apicella MA, McEwan AG, Jennings MP. 2007. Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol Microbiol. 63:54–68.10.1111/mmi.2007.63.issue-1
  • Shanks RMQ, Stella N, Kalivoda EJ, Doe MR, O’Dee DM, Lathrop KL, Guo FL, Nau GJ. 2007. A Serratia marcescens OxyR homolog mediates surface attachment and biofilm formation. J Bacteriol. 189:7262–7272.10.1128/JB.00859-07
  • Shaw SL, Long SR. 2003. Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol. 132:2196–2204.10.1104/pp.103.021113
  • Sheldon JR, Yim MS, Saliba JH, Chung WH, Wong KY, Leung KT. 2012. Role of rpoS in Escherichia coli O157:H7 strain H32 biofilm development and survival. App Environ Microbiol. 78:8331–8339.10.1128/AEM.02149-12
  • Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ, Newman DK. 2014. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science. 343:529–533.10.1126/science.1246794
  • Siddiqui R, Khan NA. 2012. Acanthamoeba is an evolutionary ancestor of macrophages: A myth or reality? Exp Parasitol. 130:95–97.10.1016/j.exppara.2011.11.005
  • Sies H. 1997. Oxidative stress: oxidants and antioxidants. Exp Physiol. 82:291–295.10.1113/expphysiol.1997.sp004024
  • Southam CM, Ehrlich J. 1943. Effects of extract of western red-cedar heartwood on certain wood-decaying fungi in culture. Phytopathol. 33:517–524.
  • Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol. 6:199–210.10.1038/nrmicro1838
  • Storz G, Imlay JA. 1999. Oxidative stress. Curr Opin Microbiol. 2:188–194.10.1016/S1369-5274(99)80033-2
  • Teal TK, Lies DP, Wold BJ, Newman DK. 2006. Spatiometabolic stratification of Shewanella oneidensis biofilms. Appl Environ Microbiol. 72:7324–7330.10.1128/AEM.01163-06
  • Thompson JR, Rivera HE, Closek CJ, Medina M. 2015. Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol. 4:1–20.
  • Tomida H, Yasufuku T, Fujii T, Kondo Y, Kai T, Anraku M. 2010. Polysaccharides as potential antioxidative compounds for extended-release matrix tablets. Carbohydrate Res. 345:82–86.10.1016/j.carres.2009.10.015
  • Van Houdt R, Michiels CW. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. J App Microbiol. 109:1117–1131.10.1111/jam.2010.109.issue-4
  • Villa F, Albanese D, Giussani B, Stewart PS, Daffonchio D, Cappitelli F. 2010. Hindering biofilm formation with zosteric acid. Biofouling. 26:739–752.10.1080/08927014.2010.511197
  • Villa F, Borgonovo G, Cappitelli F, Giussani B. 2012. Sub-lethal concentrations of Muscari comosum bulb extract suppress adhesion and induce detachment of sessile yeast cells. Biofouling. 28:1107–1117.10.1080/08927014.2012.734811
  • Villa F, Cappitelli F. 2013. Plant-derived bioactive compounds at sub-lethal concentrations: towards smart biocide-free antibiofilm strategies. Phytochem Rev. 12:245–254.10.1007/s11101-013-9286-4
  • Villa F, Pitts B, Stewart PS, Giussani B, Roncoroni S, Albanese D, Giordano C, Tunesi M, Cappitelli F. 2011. Efficacy of zosteric acid sodium salt on the yeast biofilm model Candida albicans. Microb Ecol. 62:584–598.10.1007/s00248-011-9876-x
  • Villa F, Remelli W, Forlani F, Gambino M, Landini P, Cappitelli F. 2012. Effects of chronic sub-lethal oxidative stress on biofilm formation by Azotobacter vinelandii. Biofouling. 28:823–833.10.1080/08927014.2012.715285
  • Villa F, Remelli W, Forlani F, Vitali A, Cappitelli F. 2012. Altered expression level of Escherichia coli proteins in response to treatment with the antifouling agent zosteric acid sodium salt. Environ Microbiol. 14:1753–1761.10.1111/j.1462-2920.2011.02678.x
  • Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. 2013. Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol. 11:157–168.10.1038/nrmicro2960
  • Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F. 2012. The second skin: ecological role of epibiotic biofilms on marine organisms. Front Microbiol. 3:1–21.
  • Walters MC, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother. 47:317–323.10.1128/AAC.47.1.317-323.2003
  • Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Ann Rev Cell Develop Biol. 21:319–346.10.1146/annurev.cellbio.21.012704.131001
  • Wei Q, Le Minh PN, Dötsch A, Hildebrand F, Panmanee W, Elfarash A, Schulz S, Plaisance S, Charlier D, Hassett D, et al. 2012. Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucl Acids Res. 40:4320–4333.10.1093/nar/gks017
  • Wu Y, Ding Y, Cohen Y, Cao B. 2015. Elevated level of the second messenger c-di-GMP in Comamonas testosteroni enhances biofilm formation and biofilm-based biodegradation of 3-chloroaniline. Appl Microbiol Biotechnol. 99:1967–1976.10.1007/s00253-014-6107-7
  • Wu J, Lin X, Xie H. 2008. OxyR is involved in coordinate regulation of expression of fimA and sod genes in Porphyromonas gingivalis. FEMS Microbiology Lett. 282:188–195.10.1111/fml.2008.282.issue-2
  • Wu X, Wang X, Drlica K, Zhao X. 2011. A toxin-antitoxin module in Bacillus subtilis can both mitigate and amplify effects of lethal stress. PLoS One. 6:e23909.10.1371/journal.pone.0023909
  • Wu Y, Vulić M, Keren I, Lewis K. 2012. Role of oxidative stress in persister tolerance. Antimic Agents Chemoth. 56:4922–4926.10.1128/AAC.00921-12
  • Xie K, Peng H, Hu H, Wang W, Zhang X. 2013. OxyR, an important oxidative stress regulator to phenazines production and hydrogen peroxide resistance in Pseudomonas chlororaphis GP72. Microbiol Res. 168:646–653.10.1016/j.micres.2013.05.001
  • Zhao X, Drlica K. 2014. Reactive oxygen species and the bacterial response to lethal stress. Curr Opin Microbiol. 21:1–6.10.1016/j.mib.2014.06.008
  • Zheng L, Chen Z, Itzek A, Ashby M, Kreth J. 2011. Catabolite control protein A controls hydrogen peroxide production and cell death in Streptococcus sanguinis. J Bacteriol. 193:516–526.10.1128/JB.01131-10
  • Ziegelhoffer EC, Donohue TJ. 2009. Bacterial responses to photo-oxidative stress. Nat Rev Microbiol. 7:856–863.

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