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ENCYCLOPEDIAOFVIROLOGY

FOURTHEDITION

Volume1

ENCYCLOPEDIAOFVIROLOGY

FOURTHEDITION

EDITORSINCHIEF

DennisH.Bamford

MolecularandIntegrativeBiosciencesResearchProgramme

FacultyofBiologicalandEnvironmentalSciences

UniversityofHelsinki,Helsinki,Finland

MarkZuckerman

SouthLondonSpecialistVirologyCentre

King’sCollegeHospitalNHSFoundationTrust London,UnitedKingdom and

DepartmentofInfectiousDiseases

SchoolofImmunologyandMicrobialSciences,King’sCollegeLondonMedicalSchool London,UnitedKingdom

Volume1

AcademicPressisanimprintofElsevier Radarweg29,POBox211,1000AEAmsterdam,Netherlands TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom 50HampshireStreet,5thFloor,CambridgeMA02139,UnitedStates

Copyright r 2021ElsevierLtd.unlessotherwisestated.Allrightsreserved.

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ThisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightbythePublisher(otherthanasmaybe notedherein).

Notices

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ISBN978-0-12-814515-9

Forinformationonallpublicationsvisitour websiteathttp://store.elsevier.com

Publisher:OliverWalter

AcquisitionsEditor:PriscillaBraglia

ContentProjectManager:KatarzynaMiklaszewska

AssociateContentProjectManager:GayathriS.

Designer:MatthewLimbert

EDITORSINCHIEF

DennisH.Bamford,PhD,isProfessorEmeritusofVirologyattheFacultyofBiologicaland EnvironmentalSciences,UniversityofHelsinki,Finland.HeobtainedhisPhDin1980from theDepartmentofGenetics,UniversityofHelsinki.During1981–1982hewasanEMBO postdoctoralfellowatthePublicHealthResearchInstituteoftheCityofNewYork,United States,andduring1983–1992heworkedasaSeniorScientistattheAcademyofFinland. In1993hewasappointedProfessorofGeneralMicrobiologyattheUniversityofHelsinki. HewasawardedtheesteemedAcademyProfessorshiptwice,in2002–2007and2012–2016, andhealsoservedtwiceastheDirectoroftheFinnishCenterofExcellence(inStructural Virology,2000–2005,andinVirusResearch,2006–2011).Prof.Bamfordhashadcontinuous externalresearchfunding(e.g.,fromseveralEuropeanUnion,AcademyofFinland,TEKESand JuséliusFoundationfunds,aswellastheHumanFrontierScienceProgram).HeisanEMBO memberandhasheldseveralpositionsoftrustinscientificandadministrativeorganizations. Prof.Bamfordhaspublishedapprox.400articlesininternationalpeer-reviewedjournalsin virology,microbiology,biochemistry,andmolecularbiology(36oftheminhighimpact journals).Abouthalfoftheprimaryarticleshavebeenpublishedwithinternationalcollaborators showinghighinternationalintegration.Hehasalsobeeninvitedtogive56keynoteandplenary presentationsinmajorinternationalmeetings.Prof.Bamfordhassupervisedover35Master’sand over40PhDtheses.Sevenofhisgraduatestudentsorpostdocshaveobtainedaprofessorshipandasimilarnumberhaveaprincipal investigatorstatus.Prof.Bamfordhasstudiedvirusevolutionfromastructure-centeredperspective,showingthatseeminglyunrelated viruses,suchasbacteriophagePRD1andhumanadenovirushavesimilarvirionarchitecture.Whenthecoronavirionarchitecturewas graduallyrevealed,itwasobservedthatitsstructuralelementswereclosetothoseseeninRNAbacteriophagephi6sothatphi6hasbeen activelyusedassurrogateforpathogenicviruses-quiteasurprise!

Dr.MarkZuckerman isHeadofVirology,ConsultantMedicalVirologist,andHonorarySenior LectureratSouthLondonSpecialistVirologyCentre,King’sCollegeHospitalNHSFoundation TrustandKing’sCollegeLondonMedicalSchool,DepartmentofInfectiousDiseases,Schoolof ImmunologyandMicrobialSciencesinLondon,UnitedKingdom.Hisinterestsincludethe clinicalinterfacebetweendevelopingmoleculardiagnostictestsrelevanttothelocalpopulation ofpatients,respiratoryvirusinfections,herpesvirusinfectionsinimmunocompromisedpatients andblood-bornevirustransmissionincidentsinthehealthcaresetting.HehaschairedtheUK ClinicalVirologyNetwork,RoyalCollegeofPathologistsVirologySpecialtyAdvisoryCommittee andVirologyExaminersPanelandisamemberoftheSpecialtyAdvisoryCommitteeon TransfusionTransmittedViruses.Heisaco-authoronfoureditionsofthe “Mims’ Medical Microbiology” textbook,haswrittenchaptersinanumberofothertextbooksandhasover100 publicationsininternationalpeer-reviewedjournalsandisanassociateeditorfortwojournals.

EDITORIALBOARD

EditorsinChief

DennisH.Bamford

MolecularandIntegrativeBiosciencesResearchProgramme,FacultyofBiologicalandEnvironmentalSciences,UniversityofHelsinki,Helsinki, Finland

MarkZuckerman

SouthLondonSpecialistVirologyCentre,King’sCollegeHospitalNHSFoundationTrust,London,UnitedKingdomandDepartmentof InfectiousDiseases,SchoolofImmunologyandMicrobialSciences,King’sCollegeLondonMedicalSchool,London,UnitedKingdom

SectionEditors

ClaudeM.Fauquet

StLouis,MO,UnitedStates

MichaelFeiss

DepartmentofMicrobiologyandImmunology,CarverCollegeofMedicine,UniversityofIowa,IowaCity,IA,UnitedStates

ElizabethE.Fry

DepartmentofStructuralBiology,NuffieldDepartmentofMedicine,UniversityofOxford,Oxford,UnitedKingdom

SaidA.Ghabrial†

DepartmentofPlantPathology,UniversityofKentucky,Lexington,KY,UnitedStates

EricHunter

DepartmentofPathologyandLaboratoryMedicine,EmoryUniversitySchoolofMedicineandEmoryVaccineCenter,EmoryUniversity, Atlanta,GA,UnitedStates

IlkkaJulkunen

InstituteofBiomedicine,UniversityofTurku,Turku,Finland

PeterJ.Krell

DepartmentofMolecularandCellularBiology,UniversityofGuelph,Guelph,ON,Canada

MartKrupovic

ArchaealVirologyUnit,InstitutPasteur,Paris,France

MaijaLappalainen

HUSDiagnosticCenter,HUSLAB,ClinicalMicrobiology,UniversityofHelsinkiandHelsinkiUniversityHospital,Helsinki,Finland

HubertG.M.Niesters

DepartmentofMedicalMicrobiologyandInfectionPrevention,DivisionofClinicalVirology,UniversityMedicalCenterGroningen,Groningen,TheNetherlands

MassimoPalmarini

MRC-UniversityofGlasgowCentreforVirusResearch,Glasgow,UnitedKingdom

DavidPrangishvili

InstitutPasteur,Paris,FranceandIvaneJavakhishviliTbilisiStateUniversity,Tbilisi,Georgia

DavidI.Stuart

DepartmentofStructuralBiology,NuffieldDepartmentofMedicine,UniversityofOxford,Oxford,UnitedKingdomandDiamondLight Source,Didcot,UnitedKingdom

NobuhiroSuzuki

InstituteofPlantStressandResources(IPSR),OkayamaUniversity,Kurashiki,Japan

†Deceased.

SaidA.Ghabrial† receivedhisBScin1959fromCairoUniversity,Cairo,Egypt,andhisPhD fromLouisianaStateUniversity,BatonRouge,LA,UnitedStates,in1965.Dr.Ghabrialdid postdoctoralresearchattheUniversityofCalifornia,Davis,CA,UnitedStates,beforereturning toCairo,whereheservedasaplantvirologistintheMinistryofAgriculture.Hereturnedto theUnitedStatesin1970todopostdoctoralresearchatPurdueUniversity,WestLafayette,IN. In1972,hejoinedthePlantPathologyDepartmentattheUniversityofKentucky,Lexington,KY, UnitedStates,whereherosetotherankofprofessorin1986andworkeduntil2013.

Dr.Ghabrialhasservedasanassociateandsenioreditorof Phytopathology.Heservedonthe editorialboardsoftheEncyclopediaofVirology,3rdeditionandEncyclopediaofPlantPathology,andeditedathematicissueof AdvancesinVirusResearchon “Mycoviruses”.Hewasamember oftheAmericanPhytopathologicalSociety(APS)andtheAmericanSocietyforVirology(ASV);in July2002hewaselectedasaFellowoftheAmericanPhytopathologicalSociety.Healsoactedas ChairoftheICTVSubcommitteeonFungalVirusesin1987–1993and2011–2014.

Hislongprofessionalcareerallowedhimtomakemanyscientificachievementsinphytopathologyandvirology.Amongthemaremoleculardissectionofalegume-infectingRNA virus,beanpodmottlevirus(BPMV),developmentofBPMV-basedvectors,discoveryofa transmissibledebilitationdiseaseofthephytopathogenicascomycete, Helminthosporiumvictoriae (Cochliobolusvictoriae),establishmentofaviraletiologyofthe H.victoriae disease,and advancementofstructuralbiologyofdiversefungalviruses.

EricHunter,PhD,isProfessorofPathologyandLaboratoryMedicineatEmoryUniversity, Atlanta,GA,UnitedStates.HeservesasCo-DirectoroftheEmoryCenterforAIDSResearch andisaGeorgiaResearchAllianceEminentScholar.

Dr.Hunter’sresearchfocushasbeenthemolecularvirologyandpathogenesisofretroviruses, includinghumanimmunodeficiencyvirus.Hehasmadesignificantcontributionstotheunderstandingoftheroleofretroviralglycoproteinstructuralfeaturesduringviralentryandproviding uniqueinsightsintotheassemblyandreplicationofthisvirusfamily.Inrecentyearstheemphasisof hisresearchhasbeenonHIVtransmissionandpathogenesis,definingtheextremegeneticbottleneck andselectionofviruseswithuniquetraitsduringHIVheterosexualtransmission.Hehasdescribed theselectionof fittervirusesatthetargetmucosa,agenderdifferenceintheextentofselectionbias, andaroleforgenitalinflammationinreducingselection.HisresearchhasdefinedtheimpactofHIV adaptationtothecellularimmuneresponseon immunerecognitionandcontrolofHIVafter transmission,aswellasonvirusreplicative fitnessinvitroandinvivo.Recentworkhighlightstherolesthatvirusreplicative fitnessandsex ofthehostplayindefiningdiseaseprogressioninanewlyinfectedindividual.Hisbibliographyincludesover300peer-reviewedarticles, reviews,andbookchapters.HehasalsobeentherecipientoffourNIHmeritawardsforhisworkonretrovirusandHIVmolecularbiology. Dr.HunterservedastheEditorinChiefofthejournal AIDSResearchandHumanRetroviruses for10years.HewasChairofthe AIDSVaccineResearchSubcommitteewhichischargedwithprovidingadviceandconsultationonAIDSvaccineresearchtothe NationalInstituteofAllergyandInfectiousDiseasesandcontinuestoserveoneditorialboardsforseveralacademicjournalsand onexternaladvisorycommitteesforseveralgovernment,academic,andcommercialinstitutions.

IlkkaJulkunen graduatedasanMD/PhDin1984fromtheDepartmentofVirology,Universityof Helsinki,Helsinki,Finland.HeworkedasapostdoctoralresearchfellowatMemorialSloanKetteringCancerCenterinNewYork,UnitedStates,in1986–1989,followedbypositionsasa seniorscientist,groupleaderandresearchprofessoratFinnishInstituteforHealthandWelfarein 1989–2013.In2013hebecameaProfessorofVirologyattheUniversityofTurku,Turku,Finland. TheresearchinterestsofDr.Julkunenhaveconcentratedoninnateandadaptivehumoral immunityinviralandmicrobialinfections.HehasstudiedintracellularsignalingandRIG-Iand TLR-mediatedactivationofinterferonsysteminhumanmacrophagesanddendriticcellsandstable celllinesinresponsetohumanandavianinfluenza,Sendai,Zikaandcoronavirusinfections.In addition,hehasanalyzedthedownregulationofinnateimmunitybyviralregulatoryproteinsfrom influenza,HCV, flavi-, filo-andcoronaviruses.Hehasexpertiseinvaccinology,biotechnologyand developmentofmethodstoanalyzeantiviralimmunity,hehasalsobeenactivelyinvolvedin researchtrainingandcollaborationswithbiotechnologicalindustry.

†Deceased.

PeterKrell startedhiscareerinvirologyearlyasasummerhighschoolstudentworkingforthe CanadianForestryServicestudyingtheresistanceofnuclearpolyhedrosisviruses(nowcalled baculoviruses)toenvironmentalexposurewithDr.FredT.BirdattheInsectPathologyResearch InstituteinSaultSte.Marie,ON,Canada.HereceivedhisBScandMScinbiologyfromCarleton UniversitystudyingtheiridovirusTipulaIridescentViruswithDrPeterLee,inOttawa,theCanadiancapital.ForhisPhDheheadedeasttoDalhousieUniversityinHalifax,NovaScotiaonthe Atlanticcoast.Inadditiontoenjoyingthesaltseaair,freshcod,lobsterandmussels,hestudiedthe molecularbiologyofpolydnavirusesundertheguidanceofDrDonStoltz.HeadingsouthtoTexas A&MUniversityinCollegeStation,TX,UnitedStates,asaPostdoctoralFellowheworkedwithDr. MaxSummer,ofbaculovirusfame,andDr.BradVinsoncontinuingtostudypolydnaviruses,but alsobecamesteepedintheearlydaysofmolecularbaculovirology.Hethenacceptedafaculty positionintheDepartmentofMicrobiologyandImmunologyattheUniversityofGuelphin Guelph,ON,Canada.Thereheswitchedtobaculovirusresearch,whichwasmoretractable,duein parttoavailablecellculturesandfocusedonviralDNAreplicationandfunctionalgenomics, particularlyonchitinase,cathepsinandME53.Incollaboration withDr.EvaNagyhestudiedmolecularbiologyofdifferentanimal viruses,notablyFowlAvianadenovirusesandtheirdevelopmentas vaccinevectors,butalsoonthebirnavirusinfectiouspancreatic necrosisvirus,thecoronavirusporcineendemicdiarrheavirus,fowlpoxvirusandtheparamyxovirusNewcastlediseasevirus.Hehasbeen involvedextensivelywithvirustaxonomy,beingactiveintheInternationalCommitteeonTaxonomyofViruses(ICTV)asmemberofthe Polydnaviridae and Baculoviridae studygroups,nationalrepresentativeofCanadaontheICTV,memberoftheExecutiveCommitteeforthe ICTVandChairoftheICTVInvertebrateVirusSubcommittee.Intermsofgovernance,PeterKrellwasPresidentoftheCanadianSociety ofMicrobiology,SecretaryandlaterPresidentoftheSocietyforInvertebratePathology,aswellasbeingontheEditorialBoardsofthe CanadianJournalofMicrobiology andtheASM JournalofVirology.WhileattheUniversityofGuelph,herosethroughtherankstoProfessor andiscurrentlyUniversityProfessorEmeritus.

MartKrupovic istheHeadoftheArchaealVirologyUnitintheDepartmentofMicrobiologyatthe InstitutPasteurofParis,France.HereceivedhisMScinBiochemistryin2005fromtheVilnius University,Vilnius,LithuaniaandPhDin2010ingeneralmicrobiologyfromtheUniversityof Helsinki,Helsinki,Finland.Hiscurrentresearchfocusesonthediversity,origin,andevolutionof viruses,aswellasmolecularmechanismsofvirus–hostinteractionsinarchaea.Hehaspublished over170journalarticlesandservesasaneditororontheeditorialboardsof BiologyDirect,Research inMicrobiology,ScientificReports,Virology,and VirusEvolution.HeisalsoamemberoftheExecutive CommitteeoftheInternationalCommitteeonTaxonomyofViruses(ICTV)andchairsthe ArchaealVirusesSubcommitteeoftheICTV.

MaijaLappalainen,MD,PhD,AssociateProfessorofClinicalMicrobiology,istheHeadof ClinicalMicrobiologyintheHUSDiagnosticCenter,HUSLAB,UniversityofHelsinkiand HelsinkiUniversityHospital,Helsinki,Finland.Inherthesisduringtheyears1987–1992she studiedtheincidenceanddiagnosticsofcongenitaltoxoplasmosis.AfterPhD,herresearch interesthasbeenindiagnosticclinicalvirology,viralhepatitis,respiratoryinfections,viral infectionsintheimmunocompromisedpatientsandviralinfectionsduringpregnancy.

HubertG.M.Niesters (1958)studiedbiologyandchemistryinNijmegen,theNetherlands.After obtaininghisPhDinUtrecht(Prof.dr.M.HorzinekandProf.dr.B.vanderZeijst,1987)onthe molecularepidemiologyofinfectiousbronchitisvirus,heworkedasapost-doctoralfellowwith Prof.dr.JimStraussattheCaliforniaInstituteofTechnology(Pasadena,UnitedStates)onthe replicationofAlphaviruses.HereceivedaNielsStensenfellowship(TheNetherlands)andanE.S. Gosneyfellowship(Caltech)duringthisperiod.

AfterreturningtotheNetherlands(1989),hebecamearesearchassociateinmedical microbiologyattheDiagnosticMedicalCenter(Delft)butmovedbacktoclinicalvirologyasa seniorresearchassociatein1991attheErasmusUniversityMedicalCenterRotterdam(Head Prof.dr.AbOsterhaus).From1993to2007,hewasresponsibleforthemoleculardiagnostics unit.Duringthisperiod,hewasinvolvedinthediscoveryandcharacterizationofseveralnew virusesandvariants.In2007,hebecamefullprofessoranddirectoroftheLaboratoryofClinical VirologywithintheDepartmentofMedicalMicrobiologyattheUniversityMedicalCenter GroningenandUniversityofGroningen.

Hehasbeenactivelyinvolvedintheimplementationanddevelopmentofnewtechnologieslikereal-timeampli ficationand automationwithinclinicalvirology.Hehasbeenfocusingonmoleculardiagnosticsanditsuseandtheclinicalvalueina transplantsetting,aswellasinmonitoringtreatmentofhepatitisviruses.Recently,hisinterestfocusesonrapidregionalepidemiology,automationincludingMiddleWaresolutionsformoleculardiagnostics,aswellasthecost–benefitofrapidpoint-ofimpactmoleculartesting.Specialinterestisfocusedonraisingawarenessforthedetectionofenteroviruses(enterovirusD68)and itsrelationshipwithacute flaccidmyelitis(AFM).

Since2017,heistheChairoftheexecutiveboardofQCMD(QualityControlofMolecularDiagnostics,Glasgow).Heisanauditor andteamleaderfortheDutchCouncilofAccreditationandCo-EditorinChiefofthe JournalofClinicalVirology.Heisan (co)-authorofmorethan250peer-reviewedpapers,chaptersandreviewsincludingemergingviruses,suchasenterovirusD68and hepatitisEvirus(H-index80).

Forhisentirework,hereceivedin2016the “EdNowakowskiSeniorMemorialClinicalVirologyAward” fromthePan AmericanSocietyforClinicalVirology.

MassimoPalmarini istheDirectoroftheMRC-UniversityofGlasgowCentreforVirusResearch andChairofVirologyattheUniversityofGlasgow,Glasgow,UnitedKingdom.Aveterinarianby training,hisresearchprogramsfocusonthebiology,evolutionandpathogenesisofarboviruses andthemechanismsofviruscross-speciestransmission.HisworkisfundedbytheMRCandthe WellcomeTrust.MassimoPalmarinihasbeenelectedFellowoftheAcademyofMedicalSciences, oftheRoyalSocietyofEdinburghandoftheRoyalSocietyofBiologyandhewasaWolfson-Royal SocietyResearchMeritAwardee.HeisaWellcomeTrustInvestigator.

DavidPrangishvili,PhD,HonoraryProfessorattheInstitutPasteur,Paris,France,andProfessor atTbilisiStateUniversity,Tbilisi,Georgia,isoneofthepioneersinstudiesonthebiologyof Archaeaandtheirviruses.Hisscientificcareerspansex-USSR(InstituteofMolecularBiology, Moscow;1970–1976),Georgia(GeorgianNationalAcademyofSciences,Tbilisi;1976–1991), Germany(Max-PlanckInstituteforBiochemistry,Munich;UniversityofRegensburg;1991–2004) andFrance(InstitutPasteur,Paris,2004–2020).Intheresearchgroupsheadedbyhim,several dozensofnewspeciesandeightnewfamiliesofarchaealviruseshavebeendiscoveredand characterized,whichdisplayremarkablediversityofuniquemorphotypesandexceptionalgenomecontents.Theresultsofhisresearchcontributetotheknowledgeonviraldiversityonour planetandchangethe fieldofprokaryoticvirology,leadingtothenotionthatvirusesof hyperthermophilicArchaeaformaparticulargroupintheviralworld,distinctivefromvirusesofBacteriaandEukarya,andtothe recognitionofthevirosphereofArchaeaasoneofthedistinctfeaturesofthisDomainofLife.DavidPrangishviliisamemberofthe AcademiaEuropaea,theEuropeanAcademyofMicrobiology,andtheGeorgianNationalAcademyofSciences.

FOREWORD

IamdelightedtowritetheforewordtothiswonderfulFourthEditionofthe EncyclopediaofVirology.TheThirdEditionwas publishedin2008,howtheworldhaschangedintheinterveningyears.Thereleaseoftheupdatedfourtheditioncouldnotbe moretimelyormoreprescient.Itissuperbandahugetributetotheauthors,Elsevierthepublisher,andtothebrillianteditors, DennisBamfordandMarkZuckerman.

SARS-CoV-2hasdominatedtheworldsinceitemergedin2019andaffectedeverycontinentandeveryaspectoflife.Areminder, ifitwereneeded,oftheimpactofinfectiousdiseases,theimportanceofvirologyandthevulnerabilityandinterconnectivityof ourworld.

Thereisnodoubtthatwithrapidlychangingecology,urbanization,climatechange,increasedtravel,andfragilepublichealth systems,epidemicsandpandemicswillbecomemorefrequent,morecomplexandhardertopreventandcontain.Mostofthese epidemicswillbecausedbyviruses,thoseweknowaboutandmaybeabletopredictandsomewedonotknowofthatwill emergefromanimals,plantsortheenvironment.Ourchangingclimatewillchangetheepidemiologyofviruses,theirvectorsand theinfectionstheycause,hencethecriticalimportanceofthistotallyrevisedFourthEditionofthe EncyclopediaofVirology which bringstogetherresearchandanunderstandingofvirusesinanimals,plants,bacteriaandfungi,theenvironment,andamong humans.Neverhasaholistic,one-healthunderstandingbeenmoreimportant.

Thatstartswithanunderstandingofthefundamentalsofvirology,a fieldofsciencethathasbeentransformedintheyearssince theThirdEdition.Anunderstandingtransformedbyembracingtraditional fieldsofmolecularandstructuralbiology,genomics, andinfluencedbyimmunology,genetics,pharmacologyandincreasinglybyepidemiologyandmathematics.Eventsof2020and 2021alsoshowwhyitissoimportanttointegratewithintraditionalvirologyanunderstandingoftheanimalandhumanhealth andbehavior,ofclimatechangeanditsimpactontheecologyofviruses,plantsciencesandvectors.Andwhywemustunderstand theviruseswethinkweknowwell,andthoseviruseslessextensivelystudied.Researchiscriticaltothis,researchthatpushesthe boundariesofwhatweknow,hasthehumilitytoseekanswerstothingswedonotunderstandandsharesthatknowledgewiththe widestpossiblecommunity.Thatresearchwillbemostexcitingattheinterfacebetweendisciplines,mostimpactfulwhen dynamic,open,inclusive,global,andcollaborative.

ThisiswhattheFourthEditionofthe EncyclopediaofVirology,thelargestreferencesourceofresearchinvirologysetsoutto achieve.Itisawonderfulcontributiontoacritical fieldofknowledge.Itcontainsnewchapters,everychapterrevisedandupdated byadedicatedglobalcommunitywhohavecometogethertoprovidewhatisabrilliantandinspiringreference.Itisanhonorto contributeinaverysmallwaytothetimelyreleaseoftheFourthEditionofthe EncyclopediaofVirology

JeremyFarrar

PREFACE

ThefourtheditionoftheEncyclopediaofVirologyisencyclopedic,butwewantedtomoveawayfromanalphabeticallist,apartfrom whereitwasmorelogical,toavisionthatencompassedadifferent structure.Articlesdescribing noveltrendsaswellasoriginal discoveriesinspecificsubfieldsofvirologyhavebeendistributedintoasetof fivevolumes,namelyFundamentalsofVirology,Human andAnimalViruses,PlantViruses,Bacterial,Archaeal,Fungal,AlgalandInvertebrateViruses,andDiagnosis,TreatmentandPrevention ofVirusInfections.

Wehadhopedthattheneweditionwould ‘goviral’ butitwasironicthatthetimetopublication12yearsafterthepreviousedition hadbeenmadeabitlongerduetoavirusinfection.Theworldencounteredadevastatingglobalpandemic,COVID-19,causedbyanew typeofacoronavirus,SARS-CoV-2.Scientistsinmanydisciplinesallovertheworldstartedimmediateeffortstodiscoversolutionsasto howtomitigateandstopthespreadofthepandemic.Virologymoved frombeingahighlyspecializedsubjecttooneinwhicheveryone becameavirologist,provingjusthowsignificantthedifferentaspectsofvirologyarein termsofunderstandingthenatureofviral infection.Sincethepreviousedition,thegrowthinthe fieldofgeneralvirologyhasbeenenormous,includinghugeadvancesinbasic science,identificationofnovelviruses,diagnosticmethods,treatmentandprevention.Takingthisintoaccount,theintroductionofthe articleswithintheEncyclopediaareverytimelyandcrucialforprovidingawealthofknowledgeofthelatest findingsinthe fieldof virologytoavastrangeofpeople,whetherschool students,undergraduates,postgraduates,teachers,scientists,researchers,journalists andothersinterestedininfectionsandtheconflictbetweenthehostandthepathogen.

Pandemicviruseshavebecomeaseriouspublicconcerninthechangingworld.Wecanaskourselveswhetherwehavereached thepointinwhichnaturecannolongercopewiththeconsequencesofincreasedpopulationdensityandhumanactivitiesthatare harmfultotheenvironment.Althoughseveralpandemicshavethreatenedmankindbefore,thisCOVID-19pandemichashighlightedthemassiveadverseeconomicconsequencestowardsthewellbeingofsocietyandtheimportanceofresearchinvirology. WeaimedtoproduceaMajorReferenceWorkthatdiffersinapproachtoothersandbindsallthevirologydisciplinestogether. Chaptershavebeenincludedonorigin,evolutionandemergenceofviruses,environmentalvirologyandecology,epidemiology, techniquesforstudyingviruses,virallifecycles,structure,entry,genomeandreplication,assemblyandpackagingandtaxonomyand viral–hostinteractions.Informationhasbeenincludedonallknownspeciesofvirusesinfectingbacteria,fungi,plants,vertebratesand invertebrates.Additionaltopicsincludeantiviralclassificationandexamplesoftheiruseinmanagementofinfection,diagnosticassays andvaccines,aswellastheeconomicimportanceofviraldiseasesofcropsandtheircontrol.

Thiseditionusedviralclassificationaccordingtothe9thReportoftheInternationalCommitteeonTaxonomyofVirusespublished in2012.Updatingittothe10thReportin2020wasaffectedbythepandemicandcanbefoundonlineathttp://ictv.global/report/. Wewishtoacknowledgethehardwork,interest, flexibilityandpatience,duringsuchdifficulttimesbothsociallyand professionally,ofeverybodyinvolvedintheprocessofwritingthiseditionoftheEncyclopediaofVirology,especiallyKatarzyna Miklaszewska,PriscillaBraglia,SamCroweandcolleaguesatElsevier.Wesincerelythankalltheauthorsandsectioneditorsfor theirexcellentcontributionstothisedition.

BookCoverImage:Virusesareobligateparasitesandallcellshavetheirownvirusesincreasingthetotalnumberofvirusestothe estimatedastronomicalnumberof1031 thatextendsthenumberofstarsintheuniverse.Theviralstringillustrateshowpandemic virusessurroundtheglobe.TheoriginalpicturewascreatedbyDr.NinaAtanasova(FinnishMeteorologicalInstituteandUniversityof Helsinki)andamendedbyMatthewLimbertatElsevier.

HOWTOUSETHEENCYCLOPEDIA

StructureoftheEncyclopedia

Allarticlesintheencyclopediaarearrangedthematicallyasaseriesofentrieswithinsubjects/sections,apartfromvolume2where thereitwasmorelogicaltohavearticlesarrangedalphabetically.

Therearethreefeaturestohelpyoueasily findthetopicyouareinterestedin:athematiccontentslist,afullsubjectindex,and contributors.

1.Thematiccontentslist:Thealphabeticalcontentslist,whichappearsatthefrontofeachvolume,liststheentriesintheorder thattheyappearintheencyclopedia.

2.Index:Theindexappearsattheendofvolume5andincludespagenumbersforquickreferencetotheinformationyouare lookingfor.Theindexentriesdifferentiatebetweenreferencestoawholeentry,apartofanentry,andatableor figure.

3.Contributors:Atthestartofeachvolumethereisalistoftheauthorswhocontributedtoallvolumes.

LISTOFCONTRIBUTORS

StephenT.Abedon

TheOhioStateUniversity,Mansfield,OH, UnitedStates

PeterAbrahamian

AgriculturalResearchService,USDepartmentof Agriculture,Beltsville,MD,UnitedStates

JônatasS.Abrahão

FederalUniversityofMinasGerais,BeloHorizonte, Brazil

FlorenceAbravanel

ToulouseUniversityHospital,Toulouse,Franceand ToulouseUniversityPaulSabatier,Toulouse,France

NicolaG.A.Abrescia

CenterforCooperativeResearchinBiosciences,Basque ResearchandTechnologyAlliance,Derio,Spain; Ikerbasque,BasqueFoundationforScience,Bilbao, Spain;andCenterforBiomedicalResearchintheLiver andDigestiveDiseasesNetwork,CarlosIIIHealth Institute,Madrid,Spain

GianPaoloAccotto

InstituteforSustainablePlantProtection,National ResearchCouncilofItaly,Torino,Italy

ElisabethAdderson

St.JudeChildren’sResearchHospital,Memphis,TN, UnitedStatesandUniversityofTennesseeHealth SciencesCenter,Memphis,TN,UnitedStates

MustafaAdhab

UniversityofBaghdad,Baghdad,Iraq

AlexeyA.Agranovsky LomonosovMoscowStateUniversity,Moscow,Russia

NasimAhmed

NationalInstituteforBiotechnologyandGenetic Engineering,Faisalabad,Pakistan

MaherAlRwahnih UniversityofCalifornia,Davis,CA,UnitedStates

OlufemiJ.Alabi

TexasA&MAgriLifeResearchandExtensionCenter, Weslaco,TX,UnitedStates

AurélieA.Albertini

InstituteforIntegrativeBiologyoftheCell(I2BC), FrenchAlternativeEnergiesandAtomicEnergy Commission,FrenchNationalCenterforScientific Research,Paris-SudUniversity,Universityof Paris-Saclay,Gif-sur-Yvette,France

AleksandraAlimova TheCityUniversityofNewYork(CUNY),Schoolof Medicine,TheCityCollegeofNewYork,NewYork, NY,UnitedStates

JuanC.Alonso NationalBiotechnologyCenter–SpanishNational ResearchCouncil,Madrid,Spain

ImranAmin NationalInstituteforBiotechnologyandGenetic Engineering,Faisalabad,Pakistan

StephanieE.Ander UniversityofColoradoSchoolofMedicine,Aurora,CO, UnitedStates

DanielleE.Anderson Duke-NUSMedicalSchool,Singapore,Singapore

IdaBagusAndika QingdaoAgriculturalUniversity,Qingdao,China

AnaC.d.S.P.Andrade FederalUniversityofMinasGerais,BeloHorizonte, Brazil

JuanaAngel Ponti ficalJaverianaUniversity,Bogota,Colombia

VanesaAnton-Vazquez King’sCollegeHospital,London,UnitedKingdom

GuidoAntonelli SapienzaUniversityofRome,Rome,Italy

JosefaAntón UniversityofAlicante,Alicante,Spain

NanakoAoki TokyoUniversityofAgricultureandTechnology,Fuchu, Japan

TimothyD.Appleby King’sCollegeHospital,London,UnitedKingdom

MiguelArenas DepartmentofBiochemistry,GeneticsandImmunology, UniversityofVigo,Vigo,SpainandCINBIO (BiomedicalResearchCenter),UniversityofVigo,Vigo, Spain

BasilArif LaboratoryforMolecularVirology,GreatLakesForestry Centre,SaultSteMarie,ON,Canada

VicenteArnau

InstituteforIntegrativeSystemsBiology(I2SysBio), UniversityofValencia–SpanishNationalResearch Council,Valencia,Spain

GauravArya DukeUniversity,Durham,NC,UnitedStates

LeylaAsadi UniversityofAlberta,Edmonton,AB,Canada

SassanAsgari

TheUniversityofQueensland,Brisbane,QLD,Australia

NinaS.Atanasova

FinnishMeteorologicalInstitute,Helsinki,Finlandand UniversityofHelsinki,Helsinki,Finland

HoussamAttoui

UMR1161Virologie,INRAE – FrenchNational ResearchInstituteforAgriculture,Foodand Environment,ANSES,EcoleNationaleVétérinaire d’Alfort,UniversityofParis-Est,Maisons-Alfort,France

SilviaAyora

NationalBiotechnologyCenter–SpanishNational ResearchCouncil,Madrid,Spain

WalidAzab

FreeUniversityofBerlin,Berlin,Germany

SashaR.Azar

TheUniversityofTexasMedicalBranch,Galveston,TX, UnitedStates

FengweiBai

TheUniversityofSouthernMississippi,Hattiesburg,MS, UnitedStates

DalanBailey

ThePirbrightInstitute,Pirbright,UnitedKingdom

S.C.Baker LoyolaUniversityofChicago,Maywood,IL, UnitedStates

FaustoBaldanti UniversityofPavia,Pavia,ItalyandScientificInstitute forResearch,HospitalizationandHealthcare,San MatteoPolyclinicFoundation,Pavia,Italy

LoganBanadyga

PublicHealthAgencyofCanada,Winnipeg,MB, Canada

AshleyC.Banyard

AnimalandPlantHealthAgency,Addlestone, UnitedKingdom;UniversityofWestSussex,Falmer, UnitedKingdom;andSt.George'sMedicalSchool, UniversityofLondon,London,UnitedKingdom

XiaoyongBao

TheUniversityofTexasMedicalBranch,Galveston,TX, UnitedStates

YimingBao

BeijingInstituteofGenomics,ChineseAcademyof Sciences,UniversityofChineseAcademyofSciences, Beijing,China

AlanD.T.Barrett

TheUniversityofTexasMedicalBranch,Galveston,TX, UnitedStates

DianaP.Baquero

ArchaealVirologyUnit,InstitutPasteur,Paris,France andSorbonneUniversity,Paris,France

MosheBar-Joseph AgriculturalResearchOrganization,VolcaniCenter,Bet Dagan,Israel

RachaelS.Barr

BristolRoyalHospitalforChildren,Bristol, UnitedKingdom

RalfBartenschlager HeidelbergUniversity,Heidelberg,Germany

DavidL.V.Bauer

FrancisCrickInstitute,London,UnitedKingdom

OliverW.Bayfield UniversityofYork,York,UnitedKingdom

SallyA.Baylis

Paul-Ehrlich-Institute,Langen,Germany

PhilippaM.Beard

ThePirbrightInstitute,Pirbright,UnitedKingdomandThe RoslinInstitute,UniversityofEdinburgh,UnitedKingdom

PaulBecher UniversityofVeterinaryMedicine,Hannover,Germany

BjörnBecker SaarlandUniversity,Saarbrücken,Germany

KarenL.Beemon JohnsHopkinsUniversity,Baltimore,MD,UnitedStates

MartinBeer

Friedrich-Loeffler-Institute,InselRiems,Germany

JoseMiguelBenito HealthResearchInstituteoftheJiménezDíaz Foundation,AutonomousUniversityofMadridandRey JuanCarlosUniversityHospital,Móstoles,Spain

MáriaBenko ˝ InstituteforVeterinaryMedicalResearch,Centerfor AgriculturalResearch,Budapest,Hungary

FelicityBurt

UniversityoftheFreeState,Bloemfontein,SouthAfrica

KerryS.Burton

LeamingtonSpa,UnitedKingdom

SarahJ.Butcher

UniversityofHelsinki,Helsinki,Finland

MathiasBüttner

LeipzigUniversity,Leipzig,Germany

JesseCahill

SandiaNationalLabs,Albuquerque,NM,UnitedStates

MariannaCalabretto

SapienzaUniversityofRome,Rome,Italy

ThierryCandresse

TheNationalResearchInstituteforAgriculture,Food andtheEnvironment,UniversityofBordeaux,Villenave d′Ornon,France

AlanJ.Cann

UniversityofLeicester,Leicester,UnitedKingdom

LorenzoCapucci

TheLombardyandEmiliaRomagnaExperimental ZootechnicInstitute,Brescia,Italy

IreneCarlon-Andres UniversityofOxford,Oxford,UnitedKingdom

JoséM.Casasnovas

NationalCenterforBiotechnology,SpanishNational ResearchCouncil(CSIC),Madrid,Spain

J.W.Casey

CornellUniversity,Ithaca,NY,UnitedStates

R.N.Casey

CornellUniversity,Ithaca,NY,UnitedStates

SherwoodR.Casjens

UniversityofUtah,SaltLakeCity,UT,UnitedStates

AntonellaCasola

TheUniversityofTexasMedicalBranch,Galveston,TX, UnitedStates

JoséR.Castón

NationalCenterforBiotechnology,SpanishNational ResearchCouncil,Madrid,Spain

CarlosE.Catalano

UniversityofColoradoAnschutzMedicalCampus, SkaggsSchoolofPharmacyandPharmaceutical Sciences,Aurora,CO,UnitedStates

RobertoCattaneo

MayoClinic,Rochester,MN,UnitedStates

PatriziaCavadini

TheLombardyandEmiliaRomagnaExperimental ZootechnicInstitute,Brescia,Italy

SupraneeChaiwatpongsakorn

NationwideChildren’sHospital,Columbus,OH, UnitedStates

SupriyaChakraborty

JawaharlalNehruUniversity,NewDelhi,India

Yu-ChanChao InstituteofMolecularBiology,AcademiaSinica,Taipei, Taiwan

TylerP.Chavers

CentersforDiseaseControlandPrevention,Atlanta, GA,UnitedStates

KepingChen

JiangsuUniversity,Zhenjiang,China

XiaoruiChen GenomicsResearchCenter,AcademiaSinica,Taipei, Taiwan

YanpingChen

BeeResearchLaboratory,AgriculturalResearchService, USDepartmentofAgriculture,Beltsville,MD, UnitedStates

DaynaCheng

NationalChengKungUniversity,Tainan,Taiwan

QuentinChesnais UniversityofStrasbourg,Colmar,France

SotaroChiba NagoyaUniversity,Nagoya,Japan

WahChiu

StanfordUniversity,Stanford,CA,UnitedStates

DavidChmielewski StanfordUniversity,Stanford,CA,UnitedStates

IrmaE.Cisneros

TheUniversityofTexasMedicalBranch,Galveston,TX, UnitedStates

LarkL.Coffey

UniversityofCalifornia,Davis,CA,Unitedstates

AlannaB.Cohen

RutgersUniversity,NewBrunswick,NJ,UnitedStates

JeffreyI.Cohen

LaboratoryofInfectiousDiseases,NationalInstituteof AllergyandInfectiousDiseases,NationalInstitutesof Health,Bethesda,MD,UnitedStates

SethColeman

RiceUniversity,Houston,TX,UnitedStates

MiquelColl

InstituteforResearchinBiomedicine,Barcelona,Spain andInstituteforMolecularBiologyofBarcelona, Barcelona,Spain

JohnCollinge

UCLInstituteofPrionDiseases,London, UnitedKingdom

CarinaConceicao

ThePirbrightInstitute,Pirbright,UnitedKingdom

GabrielaN.Condezo

NationalCenterforBiotechnology,SpanishNational ResearchCouncil,Madrid,Spain

MichaelaJ.Conley

MRC-UniversityofGlasgowCentreforVirusResearch, Glasgow,UnitedKingdom

CharlesACoomer

UniversityofOxford,Oxford,UnitedKingdom

AnneK.Cordes

HannoverMedicalSchool,InstituteofVirology,Hannover, Germany

MauricioCortesJr.

DepartmentofChemistry,CollegeofArtsandSciences, FortWayne,IN,UnitedStates

RobertH.A.Coutts

UniversityofHertfordshire,Hatfield,UnitedKingdom

JeffA.Cowley

CSIROLivestockIndustries,Brisbane,QLD,Australia

RobertW.Cross

TheUniversityofTexasMedicalBranch,Galveston,TX, UnitedStates

HenrykCzosnek

TheHebrewUniversityofJerusalem,Rehovot,Israel

HåkonDahle

DepartmentofBiologicalSciences,UniversityofBergen, Bergen,Norway

JanetM.Daly UniversityofNottingham,SuttonBonington, UnitedKingdom

SubhaDas

OkayamaUniversity,Kurashiki,Japan

IndranilDasgupta UniversityofDelhi,NewDelhi,India

SibnarayanDatta

DefenceResearchLaboratory,DefenceResearchand DevelopmentOrganisation(DRDO),Tezpur,Assam, India

AmyDavis StJudeChildren’sResearchHospital,Memphis,TN, UnitedStates

WilliamO.Dawson CitrusResearchandEducationCenter,LakeAlfred,FL, UnitedStatesandUniversityofFlorida,LakeAlfred,FL, UnitedStates

ErikDeClercq

RegaInstituteforMedicalResearch,KULeuven, Leuven,Belgium

RaoulJ.deGroot UtrechtUniversity,Utrecht,TheNetherlands

JuanC.delaTorre TheScrippsResearchInstitute,LaJolla,CA, UnitedStates

MarceloDelasHeras UniversityofZaragoza,Zaragoza,Spain

JulianaGabrielaSilvadeLima FederalUniversityofRioGrandedoNorte,Natal,Brazil

AthosS.deOliveira UniversityofBrasília,Brasília,Brazil

NicoleT.deStefano UniversityofFlorida,Gainesville,FL,UnitedStates GregDeakin NIAB-EMR,EastMalling,UnitedKingdom

PhilippeDelfosse UniversityofLuxembourg,Esch-sur-Alzette,Luxembourg

NatachaDelrez UniversityofLiège,Liège,Belgium

TatianaA.Demina MolecularandIntegrativeBiosciencesResearchProgram, FacultyofBiologicalandEnvironmentalSciences, UniversityofHelsinki,Helsinki,Finland

IsmailDemir

DepartmentofBiology,KaradenizTechnicalUniversity, Trabzon,Turkey

ZihniDemirbağ DepartmentofBiology,KaradenizTechnicalUniversity, Trabzon,Turkey

X.Deng LoyolaUniversityofChicago,Maywood,IL, UnitedStates

CécileDesbiez PlantPathologyUnit,INRAE – FrenchNational ResearchInstituteforAgriculture,Foodand Environment,Montfavet,France

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