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Advances in Experimental Medicine and Biology 1404 Salvador Almagro-Moreno Stefan Pukatzki Editors Vibrio spp. Infections Advances in Experimental Medicine and Biology Volume 1404 SeriesEditors WimE.Crusio,InstitutdeNeurosciencesCognitivesetIntégratives d’Aquitaine,CNRSandUniversityofBordeaux,PessacCedex,France HaidongDong,DepartmentsofUrologyandImmunology,MayoClinic, Rochester,MN,USA HeinfriedH.Radeke,InstituteofPharmacology&Toxicology,Clinicofthe GoetheUniversityFrankfurtMain,FrankfurtamMain,Hessen,Germany NimaRezaei ,ResearchCenterforImmunodeficiencies,Children’s MedicalCenter,TehranUniversityofMedicalSciences,Tehran,Iran OrtrudSteinlein,InstituteofHumanGenetics,LMUUniversityHospital, Munich,Germany JunjieXiao,CardiacRegenerationandAgeingLab,Instituteof CardiovascularSciences,SchoolofLifeScience,ShanghaiUniversity, Shanghai,China Advances in Experimental Medicine and Biology provides a platform for scientific contributions in the main disciplines of the biomedicine and the life sciences. This series publishes thematic volumes on contemporary researchintheareasofmicrobiology,immunology,neurosciences,biochem- istry, biomedical engineering, genetics, physiology, and cancer research. Covering emerging topics and techniques in basic and clinical science, it bringstogethercliniciansandresearchersfromvariousfields. Advances in Experimental Medicine and Biology has been publishing exceptionalworksinthefieldforover40years,andisindexedinSCOPUS, Medline (PubMed), EMBASE, BIOSIS, Reaxys, EMBiology, the Chemical AbstractsService(CAS),andPathwayStudio. 2021ImpactFactor:3.650(nolongerindexedinSCIEasof2022) (cid:129) Salvador Almagro-Moreno Stefan Pukatzki Editors Vibrio spp. Infections Editors SalvadorAlmagro-Moreno StefanPukatzki BurnettSchoolofBiomedicalSciences DepartmentofBiology UniversityofCentralFlorida TheCityCollegeofNewYork Orlando,FL,USA NewYork,NY,USA ISSN0065-2598 ISSN2214-8019 (electronic) AdvancesinExperimentalMedicineandBiology ISBN978-3-031-22996-1 ISBN978-3-031-22997-8 (eBook) https://doi.org/10.1007/978-3-031-22997-8 #TheEditor(s)(ifapplicable)andTheAuthor(s),underexclusivelicensetoSpringerNature SwitzerlandAG2023 Thisworkissubjecttocopyright.AllrightsaresolelyandexclusivelylicensedbythePublisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting,reuseofillustrations,recitation,broadcasting,reproductiononmicrofilmsorinany otherphysicalway,andtransmissionorinformationstorageandretrieval,electronicadaptation, computersoftware,orbysimilarordissimilarmethodologynowknownorhereafterdeveloped. Theuseofgeneraldescriptivenames,registerednames,trademarks,servicemarks,etc.inthis publication does not imply, even in the absence of a specific statement, that such names are exemptfromtherelevantprotectivelawsandregulationsandthereforefreeforgeneraluse. Thepublisher,theauthors,andtheeditorsaresafetoassumethattheadviceandinformationin thisbookarebelievedtobetrueandaccurateatthedateofpublication.Neitherthepublishernor the authors or the editors give a warranty, expressed or implied, with respect to the material containedhereinorforanyerrorsoromissionsthatmayhavebeenmade.Thepublisherremains neutralwithregardtojurisdictionalclaimsinpublishedmapsandinstitutionalaffiliations. ThisSpringerimprintispublishedbytheregisteredcompanySpringerNatureSwitzerlandAG Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Preface In this book, we cover some of the novel advances in the diverse field of Vibrio research. The intention of the selected chapters is to provide a wide range of topics including some novel areas of research that can capture the breadthofthemultidimensionalnatureofVibrioinfections:frommolecularto epidemiological. For instance, in Chap. 2, Christopher Waters and his colleaguesreviewnewinsightsintoV.choleraebiofilmsrangingfrommolec- ular biophysics to microbial ecology. Specifically, they highlight recent developments into V. cholerae biofilms structure, their ecological role in environmental survival and infection, the regulatory systems that control them,andbiomechanicalinsightsintothenatureofV.choleraebiofilms. Francis Santoriello and Stefan Pukatzki discuss the Vibrio type VI secre- tion system (T6SS) in Chap. 3. They describe the structure of the T6SS in different Vibrio species and outline how the use of different T6SS effector immunityproteinscontrolskinselection.Theysummarizethegeneticlocithat encodethestructuralelementsthatmakeuptheVibrioT6SSsandhowthese gene clusters are regulated. Finally, they provide insights on T6SS-based competitivedynamics,theroleofT6SSgeneticexchangeinthosecompetitive dynamics,androlesfortheVibrioT6SSinvirulence. InChap.4,SandraSanchezandWei-LeungNgdiscussmotilitycontrolas apossiblelinkbetweenquorumsensing(QS)andsurfaceattachmentinVibrio species.QSregulatesavarietyofbehaviorsthatareimportantforthelifecycle of many bacterial species including virulence factor production, biofilm formation, or metabolic homeostasis. Therefore, without QS, many species ofbacteriacannotsurviveintheirnaturalenvironments.Intheirchapter,they summarize several QS systems in different Vibrio species and discuss some emerging features that suggest that QS is intimately connected to motility control.TheyspeculatethattheconnectionbetweenmotilityandQSiscritical forVibriospeciestodetectsolidsurfacesforsurfaceattachment. In Chap. 5, Karl Klose and Cameron Lloyd discuss the structure and regulation of the Vibrio flagellum and its role in the virulence of pathogenic species.Theydiscussthenovelinsightsintothestructureofthisnanomachine that have recently been enabled by cryoelectron tomography. They also highlight recent genetic studies that have increased our understanding of flagellar synthesis specifically at the bacterial cell pole, temporal regulation of flagellar genes, and how it enables directional motility through run– reverse–flickcycles. v vi Preface The ever-expanding list of environmental reservoirs of pathogenic Vibrio spp. keeps increasing. In Chap. 6, Diane McDougald and her colleagues discuss the critical role of these reservoirs in disease. As natural inhabitants of aquatic environments, Vibrio species have complex interactions with the other dwellers of their native ecosystems that drive the evolution of traits contributing to their survival. These traits also contribute to their ability to invadeorcolonizeanimalandhumanhosts.Intheirchapter,theysummarize relationshipsofVibriospp.withotherorganismsintheaquaticenvironment and discuss how these interactions could potentially impact colonization of animalandhumanhosts. The emergence of choleragenic V. cholerae remains a major mystery as onlyonegroup,thepandemicgroup,iscapableofcausingcholerainhumans. InChap.7,SalvadorAlmagro-Morenoandhiscolleaguesexaminetheemer- genceofpathogenicV.choleraeandcholerapandemicdynamics.Theauthors discuss the diverse molecular mechanisms associated with the evolution of pandemicV.cholerae,includingthewell-knownmobilegeneticelementsthat encode thecritical virulence factors,andhighlight novel discoveriesthat are sheddinglightontheconstraintsbehindtheuniquedistributionofpandemic clones. Finally, they provide an overview of the cholera pandemics from an evolutionaryperspective. InChap.8,CeciliaSilva-ValenzuelaandAndrewCamilliexaminetherole ofbacteriophagesintheevolutionofpathogenicVibriosanddiscuss lessons for phage therapy. Bacteriophages were discovered over a century ago and haveplayedamajorroleasamodelsystemfortheestablishmentofmolecular biology. Despite their relative simplicity, new aspects of phage biology are consistentlybeingdiscovered,includingmechanismsforbattlingdefensesput upbytheirVibriohosts.Theauthorsdiscussthesemechanisms andcontend thatadeeperunderstandingofthearmsracebetweenVibrioandtheirphages will be important for the rational design of phage-based prophylaxis and therapiestopreventagainstthesebacterialinfections. V.vulnificuscontinuesbeinganunderestimatedyetlethalzoonoticpatho- gen. In Chap. 9, Carmen Amaro and Hector Carmona-Salido provide a comprehensive review of numerous aspects of the biology, epidemiology, andvirulencemechanismsofthispoorlyunderstoodpathogen.Theyempha- size the widespread role of horizontal gene transfer in V. vulnificus, specifi- callyvirulenceplasmids,anddrawparallelsfromaquaculturefarmstohuman health. By placing current findings in the context of climate change, they contend that fish farms act as evolutionary drivers that accelerate species evolution and the emergence of new virulent groups. They suggest that on-farm control measures should be adopted both to protect animals from vibriosis and as a public health measure to prevent the emergence of new zoonoticgroups. Over the past few decades, the importance of specific nutrients and micronutrients in the environmental survival, host colonization, and pathogenesis of V. cholerae has become increasingly clear. For instance, V. cholerae has evolved ingenious mechanisms that allow the bacterium to colonize and establish a niche in the intestine of human hosts, where it competes with commensals and other pathogenic bacteria for available Preface vii nutrients. In Chap. 10, Fidelma Boyd and her colleagues discuss the carbon andenergysourcesutilizedbyV.choleraeandthecurrentknowledgeonthe roleofnutritionandintestinalcolonizationdynamicsofthebacterium.They alsoexaminehownutritionalsignalsaffectvirulencegeneregulationandhow interactions with intestinal commensal species can affect intestinal colonization. In Chap. 11, Jyl Matson and Jay Akolkar examine the role of stress responses in pathogenic Vibrios in host and environmental survival. Patho- genic Vibrios are regularly exposed to numerous different stress-inducing agents and conditions in the aquatic environment and when colonizing a human host. Naturally, they have developed a variety of mechanisms to survive in the presence of these stressors. The authors discuss what is known about important stress responses in pathogenic Vibrio species and theircriticalroleinbacterialsurvival. Ronnie Gavilan and Jaime Martinez-Urtaza providea thoroughreviewin Chap. 12 on V. parahaemolyticus epidemiology and pathogenesis, highlighting novel insights of this emergent foodborne pathogen. They address the microbiological and genetic detection of V. parahaemolyticus, the main virulence factors, and the epidemiology of genotypes involved in foodborneoutbreaksglobally.Interestingly,theepidemiologicaldynamicsof V.parahaemolyticusinfectionsremainobscureasthediseaseischaracterized by the abrupt appearance of outbreaks in areas where the bacterium had not been previously detected. They discuss the recent studies that show the link between the appearance of epidemic outbreaks of Vibrio and environmental factors such as oceanic transport of warm waters and how recent genomic advances allow us to infer possible biogeographical patterns of V.parahaemolyticus. Duringperiodsthatarenotconduciveforgrowthorwhenfacingstressful conditions, Vibrios enter a dormant state called viable but non-culturable (VBNC). In Chap. 13, Sariqa Hagley analyzes the role of VBNC in Vibrio survival and pathogenesis and the molecular mechanisms regulating this complex phenomenon. She emphasizes some of the novel findings that make “studying the VBNC state now more exciting than ever” and its significance in the epidemiology of these pathogens and its critical role in foodsafety. One of the best studied aspects of pathogenic Vibrios are the virulence cascades that lead to the production of virulence factors and, ultimately, clinical outcomes. In Chap. 14, Jon Kull and Charles Midgett examine the regulationofVibriovirulencegenenetworksfromastructuralandbiochemi- cal perspective. The authors discuss the recent research into the numerous proteinsthatcontributetoregulatingvirulenceinVibriospp.suchasquorum sensing regulator HapR, the transcription factors AphA and AphB, or the virulence regulators ToxR and ToxT. The authors highlight how insights gained from these studies are already illuminating the basic molecular mechanisms by which the virulence cascade of pathogenic Vibrios unfolds and contend that understanding how protein interactions contribute to the host–pathogen communications will enable the development of new antivirulencecompoundsthatcaneffectivelytargetthesepathogens. viii Preface The critical role of environmental reservoirs in the distribution of pathogenic Vibrios and how they can potentially drive outbreaks are beginningto beunderstood.InChap.15,BrandonOgbunugaforandAndreaAyalaexplore theincreasinglyappreciatedcontributionofbirdsinthespreadofpathogenic Vibrios and its epidemiological consequences. To date, eleven of the twelve pathogenic Vibrio species have been isolated from aquatic and ground- foragingbirdspecies.Theauthorsdiscusstheimplicationsthatthesefindings haveforpublichealth,aswellastheOneHealthparadigm.Theycontendthat aspathogenicVibriosbecomemoreabundantthroughouttheworldasaresult ofwarmingestuariesandoceans,susceptibleavianspeciesshouldbecontin- uallymonitoredaspotentialreservoirsforthesepathogens. The first Vibrio genomes were sequenced 20 years ago revealing a func- tionalandphylogeneticdiversitypreviouslyunimaginedaswellasagenome structureindeliblyshapedbyhorizontalgenetransfer.Sincethenaplethoraof genomes from pathogenic isolates has been added to the databases and an unprecedenteddegreeofknowledgehasbeengleanedfromthem.InChap.16, Martinez-Urtaza and his colleagues highlight some of the major lessons that wehavelearnedfromVibriopathogengenomicsinthepastfewdecades.The initial glimpses into these organisms also revealed a genomic plasticity that allowedthesebacteriatothriveinchallengingandvariedaquaticandmarine environments, but critically also a suite of pathogenicity attributes. The authors outline how the advent of genomics and advances in bioinformatic anddataanalysistechniquesprovidedamorecohesiveunderstandingofhow thesepathogenshaveevolvedandemergedfromenvironmentalsources,their evolutionaryroutesthroughtimeandspace,andhowtheyinteractwithother bacteriaandthehumanhost. Orlando,FL SalvadorAlmagro-Moreno NewYork,NY StefanPukatzki Contents 1 VibrioInfectionsandtheTwenty-FirstCentury. . . . . . . . . .. 1 SalvadorAlmagro-Moreno,JaimeMartinez-Urtaza, andStefanPukatzki 2 NewInsightsintoVibriocholeraeBiofilmsfromMolecular BiophysicstoMicrobialEcology. . . .. . . . .. . . .. . . .. . . ... 17 Jung-ShenB.Tai,MicahJ.Ferrell,JingYan, andChristopherM.Waters 3 TypeVISecretionSystems:EnvironmentalandIntra-host CompetitionofVibriocholerae. . . . . . . . . . . . . . . . . . . . . . .. 41 FrancisSantorielloandStefanPukatzki 4 MotilityControlasaPossibleLinkBetweenQuorum SensingtoSurfaceAttachmentinVibrioSpecies. . . . . . . . .. 65 SandraSanchezandWai-LeungNg 5 TheVibrioPolarFlagellum:StructureandRegulation. .. . .. 77 CameronJ.LloydandKarlE.Klose 6 EnvironmentalReservoirsofPathogenicVibriospp. andTheirRoleinDisease:TheListKeepsExpanding. . . . .. 99 ParisaNoorian,M.MozammelHoque, GustavoEspinoza-Vergara,andDianeMcDougald 7 CholeraDynamicsandtheEmergenceofPandemic Vibriocholerae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 127 DeepakBalasubramanian,MarioLópez-Pérez, andSalvadorAlmagro-Moreno 8 RoleofBacteriophagesintheEvolutionofPathogenic VibriosandLessonsforPhageTherapy. . . . . . . . . . . . . . . . . 149 RobertoC.Molina-Quiroz,AndrewCamilli, andCeciliaA.Silva-Valenzuela 9 Vibriovulnificus,anUnderestimatedZoonoticPathogen. . .. 175 CarmenAmaroandHéctorCarmona-Salido ix