Table Of ContentAdvances 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
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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
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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 patho-
genesis 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 patho-
genic 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
