Stress and environmental regulation of gene expression and adaptation in bacteria Volume 1 Stress and environmental regulation of gene expression and adaptation in bacteria Volume 1 Editedby Frans J. de Bruijn INRA-CNRSLaboratoryofPlant-MicrobeInteractions(LIPM) ChemindeBordeRouge-Auzeville Castanet-Tolosan France Copyright©2016byJohnWiley&Sons,Inc.Allrightsreserved. PublishedbyJohnWiley&Sons,Inc.,Hoboken,NewJersey. PublishedsimultaneouslyinCanada. 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Regulationofgeneexpressioninbacteriaplaysakeyroleintheiradaptationtoever-changingenvironments.Transcriptionisthefirst levelofcontrolthathasbeendescribedanddecadesofresearchhaveledtoathoroughcharacterizationofthetranscriptional network,atleastforsomeofthemodelbacteriasuchasEscherichiacoli.However,itisnowclearthatmanygenesaresubjectto post-transcriptionalcontrolaswell,andsmallRNAsareamajorclassofpost-transcriptionalregulators.Manyfunctionsareinfact controlledbymixedregulatorycircuitsencompassingbothtranscriptionalandpost-transcriptionalcontrolmediatedrespectivelyby proteinsorRNAs.Thepropertiesofsuchcircuitsarejuststartingtobeelucidated.Intheregulatoryschemeshownonthecover,the involvementofHfq-bindingsRNAsincontrolofmotilityandadhesioninenterobacteriaisdepicted.Positiveandnegativecontrols areshownwithnormalandblunt-endarrowsrespectively.Asterisksindicateregulatoryinteractionspresumedtobedirect.Green triangleshighlightfeedforwardregulatorymotifs.TheregulatoryschemeisfoundinFigure5.1.1inChapter5.1byMaudeGuillier etal.FormoredetailsseeChapter5.1. 10 9 8 7 6 5 4 3 2 1 Thisworkisdedicatedtomywife,CathySenta-LoysdeBruijn,forhersupportandinterestinthe book,andherloveandunderstandingduringthehecticeditingepisodes. Contents VOLUME 1 2.10 Transposableelements:atoolkitforstressand environmentaladaptationinbacteria,137 Preface,xiii AnnaUllastres,MiriamMerenciano,LainGuio,and Acknowledgements,xiv JosefaGonza´lez Listofcontributors,xv 2.11 CRISPR–Cassystem:anewparadigmforbacterial stressresponsethroughgenomerearrangement,146 1 Introduction,1 JosephA.Hakim,HyunminKoo,JanD.vanElsas, FransJ.deBruijn JackT.Trevors,andAsimK.Bej 2.12 Thecoppermetallomeinprokaryoticcells,161 Section2: Keyoverviewchapters,3 ChristopherRensing,HendA.Alwathnani,and 2.1 Stress-inducedchangesintranscriptstability,5 SylviaF.McDevitt DvoraBiranandElioraZ.Ron 2.13 Ribonucleasesasmodulatorsofbacterialstress 2.2 StressChipformonitoringmicrobialstressresponsein response,174 theenvironment,9 Ca´tiaBa´rria,VaˆniaPobre,AfonsoM.Bravo,and JoyD.VanNostrand,AifenZhouandJizhongZhou Cec´ıliaM.Arraiano 2.3 Arevolutionaryparadigmofbacterialgenome 2.14 Double-strand-breakrepair,mutagenesis,and regulation,23 stress,185 AkiraIshihama ElizabethRogers,RaulCorrea,BrittanyBarreto, Mar´ıaAnge´licaBravoNu´n˜ez,P.J.Minnick,Diana 2.4 Roleofchangesinσ70-driventranscriptionin VeraCruz,JunXia,P.J.Hastings,andSusanM. adaptationofE.colitoconditionsofstressor Rosenberg starvation,37 UmenderK.Sharma 2.15 SigmafactorcompetitioninEscherichiacoli:kinetic andthermodynamicperspectives,196 2.5 ThedistributionandspatialorganizationofRNA KuldeepkumarRamnareshGuptaand polymeraseinEscherichiacoli:growthrateregulation DipankarChatterji andstressresponses,48 DingJunJin,CedricCagliero,JeromeIzard,Carmen 2.16 Ironhomeostasisandiron–sulfurclusterassemblyin MataMartin,andYanNingZhou Escherichiacoli,203 HuangenDing 2.6 TheECFclassification:aphylogeneticreflectionofthe regulatorydiversityintheextracytoplasmicfunctionσ 2.17 Mechanismsunderlyingtheantimicrobialcapacityof factorproteinfamily,64 metals,215 DanielaPintoandThorstenMascher JoeA.LemireandRaymondJ.Turner 2.7 Toxin–antitoxinsystemsinbacteriaandarchaea,97 2.18 Acyl-homoserinelactone-basedquorumsensingin YoshihiroYamaguchiandMasayoriInouye membersofthemarinebacterialRoseobacterclade: complexcell-to-cellcommunicationcontrolsmultiple 2.8 BacterialsRNAs:regulationinstress,108 physiologies,225 MarimuthuCitartan,CarstenA.Raabe,Chee-Hock AlisonBuchan,AprilMitchell,W.NathanCude, Hoe,TimofeyS.Rozhdestvensky,andThean-Hock andShawnCampagna Tang 2.19 Nativeandsyntheticgeneregulationtonitrogen 2.9 Bacterialstressresponsesasdeterminantsof limitationstress,234 antimicrobialresistance,115 Jo¨rgSchumacher MichaelFruciandKeithPoole vii viii Contents Section3: One-,two-,andthree-component 4.7 Posttranslationalregulationofantisigmafactorsof regulatorysystemsandstressresponses,247 RpoE:acomparisonbetweentheEscherichiacoliand Pseudomonasaeruginosasystems,361 3.1 Two-componentsystemsthatcontroltheexpressionof SundarPandey,KyleL.Martins,andKalaiMathee aromatichydrocarbondegradationpathways,249 TinoKrell Section5: SmallnoncodingRNAsandstress 3.2 Cross-talkofglobalregulatorsinStreptomyces,257 responses,369 JuanF.Mart´ın,FernandoSantos-Beneit,Alberto Sola-Landa,andPalomaLiras 5.1 BacterialsmallRNAsinmixedregulatorycircuits,371 JonathanJagodnik,DenisThieffry,andMaude 3.3 NO–H-NOX-regulatedtwo-componentsignaling,268 Guillier DhruvP.Arora,SandhyaMuralidharan,and ElizabethM.Boon 5.2 RoleofsmallRNAsinPseudomonasaeruginosa virulenceandadaptation,383 3.4 Thetwo-componentCheYsysteminthechemotaxisof HansiKumari,DeepakBalasubramanian,andKalai Sinorhizobiummeliloti,277 Mathee MartinHaslbeck 5.3 Physiologicaleffectsofposttranscriptionalregulation 3.5 Stimulusperceptionbyhistidinekinases,282 bythesmallRNASgrSduringmetabolicstressin HannahSchramke,YangWang,RalfHeermann,and Escherichiacoli,393 KirstenJung GregoryR.Richards Section4: Sigmafactorsandstressresponses,301 5.4 ThreerpoS-activatingsmallRNAsinpathways contributingtoacidresistanceofEscherichiacoli,402 4.1 TheextracytoplasmicfunctionsigmafactorEcfO GeunuBak,KookHan,DaunKim,Kwang-sunKim, protectsBacteroidesfragilisagainstoxidativestress,303 andYounghoonLee IvanC.Ndamukong,SamanthaPalethorpe,Michael Betteken,andC.JeffreySmith 5.5 ThermalstressnoncodingRNAsinprokaryotesand eukaryotes:acomparativeapproach,412 4.2 Regulationofenergymetabolismbythe MercedesdelaFuenteandJose´Luis extracytoplasmicfunction(ECF)σfactorsof Mart´ınez-Guitarte Arcobacterbutzleri,311 IratiMartinez-Malaxetxebarria,RudyMuts,Linda vanDijk,CraigT.Parker,WilliamG.Miller,Steven Section6: Toxin-antitoxinsystemsandstress Huynh,WimGaastra,JosP.M.vanPutten,Aurora responses,423 Fernandez-Astorga,andMarcM.S.MWo¨sten 6.1 Epigeneticsmediatedbyrestrictionmodification 4.3 Extracytoplasmicfunctionsigmafactorsandstress systems,425 responsesinCorynebacterium IwonaMrukandIchizoKobayashi pseudotuberculosis,321 ThiagoL.P.Castro,NubiaSeyffert,AnneC.Pinto, 6.2 Toxin–antitoxinsystemsasregulatorsofbacterial ArturSilva,VascoAzevedo,andLuisG.C.Pacheco fitnessandvirulence,437 BrittanyA.FlemingandMatthewA.Mulvey 4.4 Thecomplexrolesandregulationofstressresponseσ factorsinStreptomycescoelicolor,328 6.3 Mechanismsofstress-activatedpersisterformationin JanKormanec,BeatricaSevcikova,RenataNovakova, Escherichiacoli,446 DagmarHomerova,BronislavaRezuchova,andErik StephanieM.AmatoandMarkP.Brynildsen Mingyar 6.4 IdentificationandcharacterizationoftypeII 4.5 Proteolyticactivationofextracytoplasmicfunction toxin–antitoxinsystemsintheopportunisticpathogen (ECF)σfactors,344 Acinetobacterbaumannii,454 JessicaL.HastieandCraigD.Ellermeier EditaSuzˇiede˙liene˙,MildaJure˙naite˙,andJulija Armalyte˙ 4.6 TheECFfamilysigmafactorσHinCorynebacterium glutamicumcontrolsthethiol-oxidativestress 6.5 Transcriptionalcontroloftoxin–antitoxinexpression: response,352 keepingtoxinsunderwrapsuntilthetimeisright,463 TobiasBuscheandJo¨rnKalinowski BarbaraKeℷdzierskaandFinbarrHayes Contents ix 6.6 OppositeeffectsofGraTtoxinonstresstolerance 9.3 HowalargegenenetworkcouplesmutagenicDNA ofPseudomonasputida,473 breakrepairtostressinEscherichiacoli,570 RitaHo˜rakandHedvigTamman ElizabethRogers,P.J.Hastings,Mar´ıaAnge´licaBravo Nu´n˜ez,andSusanM.Rosenberg Section7: Stringentresponsetostress,479 9.4 Double-strandDNAbreakrepairinmycobacteria,577 7.1 PreferentialcellularaccumulationofppGpporpppGpp RichaGuptaandMichaelS.Glickman inEscherichiacoli,481 K.PotrykusandM.Cashel Section10: Adaptationtooxidativestress,587 7.2 GlobalRsh-dependenttranscriptionprofileofBrucella 10.1 Peroxide-sensingtranscriptionalregulatorsin suisduringstringentresponseunravelsadaptationto bacteria,589 nutrientstarvationandcross-talkwithotherstress JamesM.DubbsandSkornMongkolsuk responses,489 StephanKo¨hler,NabilHanna,Safia 10.2 Regulationofoxidativestress–relatedgenesimplicated Ouahrani-Bettache,KennethL.Drake,L.Garry intheestablishmentofopportunisticinfectionsby Adams,andAlessandraOcchialini Bacteroidesfragilis,603 FelipeLopesTeixeira,ReginaMariaCavalcanti 7.3 Thestringentresponseandantioxidantdefencesin PilottoDomingues,andLeandroAraujoLobo Pseudomonasaeruginosa,500 GowthamiSampathkumar,MalikaKhakimova,Tevy 10.3 Investigationintooxidativestressresponseof Chan,andDaoNguyen Shewanellaoneidensisrevealsadistinctmechanism,609 JieYuan,FenWan,andHaichunGao 7.4 MolecularbasisofthestringentresponseinVibrio cholerae,507 10.4 Anomicsviewontheresponsetosingletoxygen,619 ShreyaDasgupta,BhabatoshDas,PallabiBasu,and BorkA.BerghoffandGabrieleKlug RupakK.Bhadra 10.5 Regulatorsofoxidativestressresponsegenesin Escherichiacoliandtheirconservationinbacteria,632 Section8: ResponsestoUVirradiation,517 HerbE.Schellhorn,MohammadMohiuddin,Sarah 8.1 UVstress-responsivegenesassociatedwith M.Hammond,andStevenBotts enterobacterialintegrativeconjugativeelementsofthe 10.6 HydrogenperoxideresistanceinBifidobacterium ICESXT/R391group,519 animalissubsp.lactisandBifidobacteriumlongum,638 PatriciaArmshawandJ.TonyPembroke TaylorS.ObergandJeffR.Broadbent 8.2 AlteredoutermembraneproteinsinresponsetoUVC radiationinVibrioparahaemolyticus andVibrioalginolyticus,528 Section11: Adaptationtoosmoticstress,647 FethiBenAbdallah 11.1 Interstrainvariationinthephysiologicaland 8.3 Ultraviolet-Bradiationeffectsonthecommunity, transcriptionalresponsesofPseudomonassyringae physiology,andmineralizationofmagnetotactic toosmoticstress,649 bacteria,532 GwynA.Beattie,ChiliangChen,LindseyNielsen, YingzhaoWangandYongxinPan andBrianC.Freeman 8.4 Nucleotideexcisionrepairsystemandgeneexpression 11.2 ManagementofosmoticstressbyBacillussubtilis: inMycobacteriumsmegmatis,545 geneticsandphysiology,657 AngelinaCordone TamaraHoffmannandErhardBremer 11.3 HyperosmoticresponseofStreptococcusmutans: Section9: SOSanddoublestrandedrepairsystems frommicroscopicphysiologytotranscriptomic andstress,551 profile,677 9.1 TheSOSresponsemodulatesbacterialpathogenesis,553 LuWangandXinXu DarjaZˇgurBertok 11.4 Defectiveribosomematurationorfunctionmakes 9.2 RNAPsecondary-channelinteractorsinEscherichia Escherichiacolicellssalt-resistant,687 coli:makersandbreakersofgenomestability,561 HyoutaHimeno,TakefusaTarusawa,ShionIto,and PriyaSivaramakrishnanandChristopheHerman SimonGoto x Contents Section12: Dessicationtoleranceanddrought 14.3 Coevolutionanalysisilluminatestheevolutionary stress,693 plasticityofthechaperoninsystemGroES/L,796 MarioA.Fares 12.1 Consequencesofelevatedsaltconcentrationson expressionprofilesintherhizobiumS.meliloti1021 14.4 ClpLATPase:anovelchaperoneinbacterialstress likelyinvolvedinheatanddesiccationstress,695 responses,812 JanA.C.Vriezen,CarolineM.Finn,andKlaus PratickKharaandIndranilBiswas Nu¨sslein 14.5 DuplicatedgroELgenesinMyxococcusxanthus 12.2 Genesinvolvedintheformationofdesiccation- DK1622,820 resistantcystsinAzotobactervinelandii,709 YanWang,Xiao-jingChen,andYue-zhongLi GuadalupeEsp´ın 12.3 OsmoticanddesiccationtoleranceinEscherichiacoli Section15: Coldshockresponses,827 O157:H7andSalmonellaentericarequiresrpoS (σ38),716 15.1 Generegulationbycoldshockproteinsvia ZachPratt,MeganShiroda,AndrewJ.Stasic,Josh transcriptionantitermination,829 Lensmire,andC.W.Kaspar SangitaPhadtareandKonstantinSeverinov 12.4 DesiccationofSalmonellaentericainduces 15.2 Metagenomicanalysisofmicrobialcoldstressproteins cross-tolerancetootherstresses,725 inpolarlacustrineecosystems,837 ShlomoSela(Saldinger)andChellaiahEdwardRaja HyunminKoo,JosephA.Hakim,and Index,i1 AsimK.Bej 15.3 Roleoftwo-componentsystemsincoldtoleranceof VOLUME 2 Clostridiumbotulinum,845 Yag˘murDerman,EliasDahlsten,andHannu Preface,xiii Korkeala Acknowledgements,xiv 15.4 ColdshockCspAproteinproductionduringperiodic Listofcontributors,xv temperaturecyclinginEscherichiacoli,854 DavidStoparandTinaIvancic Section13: Heatshockresponses,737 13.1 Heatshockresponseinbacteriawithlargegenomes: 15.5 ColdshockresponseinEscherichiacoli:amodel lessonsfromrhizobia,739 systemtostudyposttranscriptionalregulation,859 AnaAlexandreandSolangeOliveira AnnaMariaGiuliodori 13.2 Smallheatshockproteinsinbacteria,747 15.6 Newinsightintocoldshockproteins: MartinHaslbeck RNA-bindingproteinsinvolvedinstressresponseand 13.3 Transcriptomeanalysisofbacterialresponsetoheat virulence,873 shockusingnext-generationsequencing,754 CharlotteMichauxandJean-Christophe Kok-GanChan Giard 13.4 Comparativeanalysesofbacterialtranscriptome 15.7 Lightregulationofcoldstressresponsesin reorganisationinresponsetotemperatureincrease,757 Synechocystis,881 Bei-WenYingandTetsuyaYomo KirillS.MironovandDmitryA.Los 13.5 ParticipationofSer–Thrproteinkinasesinregulation 15.8 Escherichiacolicoldshockgeneprofilesinresponse ofheatstressresponsesinSynechocystis,766 tooverexpressionordeletionofCsdA,RNaseR,and AnnaA.Zorina,GalinaV.Novikova,and PNPaseandrelevancetolow-temperatureRNA DmitryA.Los metabolism,890 Section14: Chaperoninsandstress,781 SangitaPhadtare 14.1 GroEL/ESchaperonin:unfoldingandrefolding reactions,783 Section16: Adaptationtoacidstress,897 VictorV.Marchenkov,NataliyaA.Ryabova,Olga 16.1 Acid-adaptiveresponsesofStreptococcusmutans, M.Selivanova,andGennadyV.Semisotnov andmechanismsofintegrationwithoxidative 14.2 FunctionalcomparisonbetweentheDnaKchaperone stress,899 systemsofStreptococcusintermediusand RobertG.QuiveyJr.,RobertaC.Faustoferri, Escherichiacoli,791 BrendalizSantiago,JonathonBaker,Benjamin ToshifumiTomoyasuandHideakiNagamune Cross,andJinXiao Contents xi 16.2 Acidsurvivalmechanismsinneutralophilic 18.3 Promiscuousfunctionsofcellenvelopestress-sensing bacteria,911 systemsinKlebsiellapneumoniaeandAcinetobacter EugeniaPennacchietti,FabioGiovannercole,and baumannii,1031 DanielaDeBiase VijayaBharathiSrinivasanandGovindan Rajamohan 16.3 Two-componentsystemsinsensingandadaptingto acidstressinEscherichiacoli,927 18.4 InfluenceofBrpAandPsroncellenvelope YokoEguchiandRyutaroUtsumi homeostasisandvirulenceofStreptococcus mutans,1043 16.4 Slr1909,anoveltwo-componentresponseregulator ZezhangT.Wen,JacobP.Bitoun,SumeiLiao,and involvedinacidtoleranceinSynechocystis JacquelineAbranches sp.PCC6803,935 LeiChen,QiangRen,JiangxinWang,andWeiwen 18.5 Modulatorsofthebacterialtwo-componentsystems Zhang involvedinenvelopestress,transport,andvirulence,1055 RajeevMisra 16.5 Comparativemassspectrometry–basedproteomicsto elucidatetheacidstressresponseinLactobacillus Section19: Ironhomeostasis,1065 plantarum,944 TiaanHeunis,ShellyDeane,andLeonM.T.Dicks 19.1 Ironhomeostasisandenvironmentalresponsesin cyanobacteria:regulatorynetworksinvolvingFur,1067 Section17: Adaptationtonitrosativestress,953 Mar´ıaLuisaPeleato,Mar´ıaTeresaBes,andMar´ıaF. 17.1 Transcriptionalregulationbythiol-basedsensorsof Fillat oxidativeandnitrosativestress,955 19.2 InterplaybetweenO andironingeneexpression: 2 TimothyTapscott,MatthewA.Crawford,and environmentalsensingbyFNR,ArcA,andFurin Andre´sVa´zquez-Torres bacteria,1079 17.2 HaemoglobinsofMycobacteriumtuberculosisand BryanTroxellandHosniM.Hassan theirinvolvementinmanagementofenvironmental 19.3 Theiron–sulfurclusterbiosynthesisregulatorIscR stress,967 contributestoironhomeostasisandresistanceto KanakL.Dikshit oxidantsinPseudomonasaeruginosa,1090 17.3 WhatisitaboutNOthatyoudon’tunderstand?The AdisakRomsang,JamesM.Dubbs,andSkorn roleofhemeandHcpRinPorphyromonas Mongkolsuk gingivalis’sresponsetonitrate(NO ),nitrite(NO ), 3 2 19.4 Transcriptionalanalysisofiron-responsiveregulatory andnitricoxide(NO),976 networksinCaulobactercrescentus,1103 JaninaP.LewisandBenjaminR.Belvin Jose´F.daSilvaNeto 17.4 Di-ironRICs:playersinnitrosative-oxidativestress 19.5 Protein–proteininteractionsregulatethereleaseof defences,989 ironstoredinbacterioferritin,1109 L´ıgiaS.NobreandL´ıgiaM.Saraiva HuiliYao,YanWang,andMarioRivera 17.5 TheVibriocholeraestressresponse:anelaborate 19.6 Proteindynamicsandiontrafficinbacterioferritin systemgearedtowardovercominghostdefenses function:amoleculardynamicssimulationstudyon duringinfection,997 wild-typeandmutantPseudomonasaeruginosa Karl-GustavRueggebergandJunZhu BfrB,1118 17.6 Ensemblemodelingenablesquantitativeexploration HuanRui,MarioRivera,andWonpilIm ofbacterialnitricoxidestressnetworks,1009 JonathanL.RobinsonandMarkP.Brynildsen Section20: Metalresistance,1131 Section18: Adaptationtocellenvelopestress,1015 20.1 Nickeltoxicity,regulation,andresistancein bacteria,1133 18.1 TheCpxinnermembranestressresponse,1017 LeeMacomberandRobertP.Hausinger RandiL.GuestandTracyL.Raivio 20.2 MetabolicnetworkstocounterAltoxicity 18.2 Newinsightsintostimulusdetectionandsignal inPseudomonasfluorescens:aholisticview,1145 propagationbytheCpx-envelopestresssystem,1025 ChristopherAuger,NishmaD.Appanna,andVasu PatrickHoernschemeyerandSabineHunke D.Appanna