Tomás G. Villa · Miguel Viñas Editors Horizontal Gene Transfer Breaking Borders Between Living Kingdoms Horizontal Gene Transfer (cid:129) Tomás G. Villa Miguel Viñas Editors Horizontal Gene Transfer Breaking Borders Between Living Kingdoms Editors TomásG.Villa MiguelViñas FacultyofPharmacy, FacultyofMedicine DepartmentofMicrobiology UniversityofBarcelona UniversityofSantiagodeCompostela Barcelona,Spain SantiagodeCompostela,Spain ISBN978-3-030-21861-4 ISBN978-3-030-21862-1 (eBook) https://doi.org/10.1007/978-3-030-21862-1 ©SpringerNatureSwitzerlandAG2019 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartofthe materialisconcerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,recitation, broadcasting,reproductiononmicrofilmsorinanyotherphysicalway,andtransmissionorinformation storageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilarmethodology nowknownorhereafterdeveloped. Theuseofgeneraldescriptivenames,registerednames,trademarks,servicemarks,etc.inthispublication doesnotimply,evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfromtherelevant protectivelawsandregulationsandthereforefreeforgeneraluse. The publisher, the authors, and the editorsare safeto assume that the adviceand informationin this bookarebelievedtobetrueandaccurateatthedateofpublication.Neitherthepublishernortheauthorsor theeditorsgiveawarranty,expressorimplied,withrespecttothematerialcontainedhereinorforany errorsoromissionsthatmayhavebeenmade.Thepublisherremainsneutralwithregardtojurisdictional claimsinpublishedmapsandinstitutionalaffiliations. ThisSpringerimprintispublishedbytheregisteredcompanySpringerNatureSwitzerlandAG. Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Contents PartI HorizontalGeneTransferAmongBacteriaandBacteriophages HorizontalGeneTransferinBacteria,anOverviewofthe MechanismsInvolved. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 T.G.Villa,L.Feijoo-Siota,A.Sánchez-Pérez,JL.R.Rama,andC.Sieiro AlternativeWaystoExchangeDNA:UnconventionalConjugation AmongBacteria. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77 AlbaBlesaandJoséBerenguer HorizontalGeneTransferBetweenBacteriophagesandBacteria: AntibioticResistancesandToxinProduction. . . . . . . . . . . . . . . . . . . . . 97 T.G.Villa,L.Feijoo-Siota,JL.R.Rama,A.Sánchez-Pérez,andM.Viñas GenomicIslandsandtheEvolutionofMultidrug-ResistantBacteria. . . . 143 MarioJuhas HorizontalGeneTransferandGenomeEvolutioninthePhylum Actinobacteria. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 CooperJ.Park,JoshuaT.Smith,andCherylP.Andam Photobacteriumdamselae:HowHorizontalGeneTransferShaped TwoDifferentPathogenicLifestylesinaMarineBacterium. . . . . . . . . . 175 CarlosR.Osorio PartII HorizontalGeneTransferBetweenBacteriaandAnimals, Plants,AmoebaandFungi HorizontalGeneTransferinMetazoa:ExamplesandMethods. . . . . . . 203 YukiYoshida,ReubenW.Nowell,KazuharuArakawa,andMarkBlaxter HorizontalGeneTransferBetweenWolbachiaandAnimals. . . . . . . . . . 227 TrinidaddeMiguel,OudeZhu,andTomásG.Villa v vi Contents HorizontalGeneTransferinObligateParasites. . . . . . . . . . . . . . . . . . . 235 J.M.Ageitos,M.Viñas,andT.G.Villa AssociationBetweenHorizontalGeneTransferandAdaptation ofGastricHumanPathogenHelicobacterpyloritotheHost. . . . . . . . . . 257 SurekhaChallaandNageswaraRaoReddyNeelapu TheRhizobiaceaeBacteriaTransferringGenestoHigherPlants. . . . . . 269 Martha-HelenaRamírez-Bahena,AlvaroPeix,andEncarnaVelázquez RoleofHorizontalGeneTransferinEvolutionofthePlantGenome. . . . 291 NageswaraRaoReddyNeelapu,MalayRanjanMishra,TitashDutta, andSurekhaChalla FungalHorizontalGeneTransfer:AHistoryBeyondthePhylogenetic Kingdoms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315 CarlosBarreiro,SantiagoGutiérrez,andElíasR.Olivera TransferofSecondaryMetaboliteGeneClusters:Assemblyand Reorganizationoftheβ-LactamGeneClusterfromBacteriato FungiandArthropods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 337 J.F.MartínandP.Liras HorizontalGeneTransferAmongNeisseriaSpeciesandHumans. . . . . 361 S.Sánchez,T.deMiguel,T.G.Villa,A.R.Gorringe,andI.M.Feavers ImplicationsofLateralorHorizontalGeneTransferfromBacteria totheHumanGastrointestinalSystemforCancerDevelopmentand Treatment. . . . .. . . .. . . .. . . .. . . . .. . . .. . . .. . . .. . . . .. . . .. . . .. 377 A.G.Abril,P.G.Lanzi,andV.Notario RoleofHorizontalGeneTransferinCancerProgression. . . . . . . . . . . . 399 A.G.AbrilandV.Notario Part I Horizontal Gene Transfer Among Bacteria and Bacteriophages Horizontal Gene Transfer in Bacteria, an Overview of the Mechanisms Involved T.G.Villa,L.Feijoo-Siota,A.Sánchez-Pérez,JL.R.Rama,andC.Sieiro Abstract Bacterialtransformation,transduction,and“conjugation”canbeconsid- eredthefirsthorizontaltransfermechanismsinlivingorganisms;thesemechanisms haveoccurredsincetheoriginofbacteriaandarestillcurrent.Althoughmechanis- tically quite different, the three processes aim to achieve the main objective of all cells, the ability to survive and adapt to new environments. Transformation, trans- duction,and“conjugation”implementDNArecombination,creatinggeneticdiver- sityand,hence,allowingbacteriatoacquirenewcapabilitiesandevolve,resultingin additional, improved, environmental adaptations that enhance bacterial survival. This chapter summarizes old paradigms and novel findings in these three genetic processesandincludesthelatestresearchontherecentlydescribedvesicle-mediated bacterialcommunicationmechanism. Keywords Horizontalgenetransfer·Bacterialtransformation·Transduction· Conjugation·Bacterialvesicles 1 Introduction Horizontal gene transfer (HGT) was not even suspected to occur in the bacterial world a century ago, although there were already a variety of data indicating its existence.Itwasthenalreadyestablished,forexample,thatbacteriacanchangetheir pathogenicityprofile,altertheirabilitytoutilizedifferentnutrients,ormodifytheir physiology to form biofilms in response to different factors (these biofilms were notedtooccasionallybreakdown,bysomeunknownmechanism).Inthemajorityof T.G.Villa(*)·L.Feijoo-Siota·JL.R.Rama FacultyofPharmacy,DepartmentofMicrobiology,UniversityofSantiagodeCompostela, SantiagodeCompostela,ACoruña,Spain A.Sánchez-Pérez FacultyofVeterinaryScience,UniversityofSydney,Sydney,NSW,Australia C.Sieiro FacultyofSciences,DepartmentofMicrobiology,UniversityofVigo,Vigo,Pontevedra,Spain ©SpringerNatureSwitzerlandAG2019 3 T.G.Villa,M.Viñas(eds.),HorizontalGeneTransfer, https://doi.org/10.1007/978-3-030-21862-1_1 4 T.G.Villaetal. cases, biofilm breakage is accompanied by the release of cytoplasmic contents, includinggenomicDNA(Maetal.2009),whichcancontributenotonlytobacterial antibioticresistance(Tetzetal.2009;SadykovandBayles2012)butalsopromote horizontalgenetransfer(MolinandTolker-Nielsen2003). WhenAvery,MacLeod,andMcCartyunraveled,in1944,thechemicalnatureof theGriffith’s“transformationprinciple,”theynotonlydiscoveredthegeneticbasis of inheritance but also shed light into the many then unknown aspects of bacterial genetics. In fact, the main conclusion of their publication was: “The evidence presented supports the belief that a nucleic acid of the desoxyribose type is the fundamentalunitofthetransformingprincipleofPneumococcusTypeIII.” ThestoryofthebacterialtransformationprocessstartedinEnglandwithFrederick Griffith(1879–1941)who,after8yearsoflongandpatientwork,published(1928)one ofthemostpivotalpapersinmicrobiology.Hisarticle,thatisknownworldwideasthe Griffith’s experiment, reported that he successfully transformed an attenuated, nonencapsulated (denominated R, for rough colonies) bacteria into a fully encapsu- lated, virulent (known as S, for smooth colonies) strain. He, nonetheless, could not identify the chemical nature of the transforming principle. Griffith’s results were confirmedthesameyearbyDawson(1928),who2yearslater(Dawson1930)further expandedhisresearchonthetransformationofS.pneumococci.Theseearlypublica- tionsonthestreptococcaltransformationprocesswerefollowedbynumerousothers, many originating from Dawson’s group at the Rockefeller Institute for Medical ResearchintheUSA,whicharecurrentlyoverlookedbymicrobiologists(forinstance, the publications in 1923 by Heidelberger and Avery and in 1923 by Avery and Heidelberger, as well as the 1925 article by Avery et al.). Genetic transformation is notidenticalinalltypesofbacteria,infactthereareprofounddifferencesbetweenthis processinGram-positiveandGram-negativeorganisms,seebelow. Research carried out in the second half of the twentieth century demonstrated a high complexity in bacterial genomes. In this manner, a typical bacterium can contain, in addition to its own chromosome, several replicons that are capable of interacting with one another and even form stable co-integrates. They include not only plasmids but also bacteriophages that can integrate into the bacterial chromo- someeitheratspecificpoints,suchasbacteriophageλ,oratdifferentpositions(i.e., P2). In addition, some replicons can integrate virtually anywhere in the bacterial chromosome and can, hence, originate a variety of different mutations, some of whicharelethaltothebacterialhost(i.e.,Mubacteriophage). For many years, bacterial transformation constituted the only horizontal gene transfer process fully demonstrated and documented in nature. But in the 1940s, a secondprocesswasdescribedbyLederbergandTatum(1946),whodenominatedit “bacterialconjugation”,asitwasreminiscent ofthe“true”eukaryoticconjugation; althoughitrequiresphysicalcontactbetweenbothpartners,itinvolvesthetransferof a single chain of double-stranded DNA. It was initially thought that all bacterial conjugationfollowedthemodelofE.coli(Wollmanetal.1956),but,infact,there aremanytypesofbacterialconjugation,andsomeofthemareexceedinglydifferent fromtheprocessundergonebyEnterobacteriaceae. Transduction,thethirdclassicalwayofHGTinbacteria,ismediatedbybacterial viruses, known as bacteriophages or phages. Although bacteriophages were HorizontalGeneTransferinBacteria,anOverviewoftheMechanismsInvolved 5 discoveredatthebeginningofthetwentiethcenturybyTwort(1915)andD’Herelle (1917), their ability to transfer genetic material was not recognized until 1952. Norton Zinder and Joshua Lederberg (1952) demonstrated that these subcellular structurescantransfergeneticpropertiesbetweendifferentbacterialstrains,andeven between unrelated bacterial species. Zinder and Lederberg concluded: “The mech- anismofgeneticexchangefoundintheseexperimentsdiffersfromsexualrecombi- nation in E. coli in many respects so as to warrant a new descriptive term, transduction.”Inaddition,thesenewultramicroscopicviruses,asTwortreferredto them, were soon used in the therapy of certain bacterial diseases, such as in the treatment of bacterial dysentery. It must be noted that all three mechanisms, trans- formation, transduction, and conjugation, are limited by restriction-modification (R-M) systems. This means that, for naked DNA or a phage DNA to be protected fromdegradationbytherecipientstrainrestrictases,itmustbederivedfromahost possessingthesameR-Msystemastherecipientbacteria,henceprotectingtheDNA bymethylation.This,inturn,determineshowquicklygeneticmarkersaretransmit- ted by HGT. Transmission is fast for DNA protected from degradation, while unprotected DNA is disseminated at a much slower rate. In accordance, the restriction-modification (R-M) system can potentially hinder bacterial HGT, as indicated by Johnston et al. in 2013. In fact, while the three HGT mechanisms increase genetic diversity, the R-M system is set to minimize bacterial genetic diversity, by degrading foreign DNA to protect bacteria from either bacteriophage infection or from naked DNA that could have a detrimental effect on the recipient strain. 2 Transformation This chapter will only address “natural” bacterial transformation, defined as an exceptional ability of certain bacteria to accept naked DNA (either dsDNA or ssDNA; Miao and Guild 1970). This precludes the inclusion of bacteria, such as Escherichiacoli,lackingthatnaturalprocess,althoughtheyareofgreatimportance tomicrobiologistsandbiotechnologists. A review of the literature on genetics and microbiology in the early twentieth centuryrevealsthatthescientistsofthetimewereconstantlyfocusingtheirattention onthefactthatbacteriainpureculturecouldundergodramatictransformations,not onlyintheirmetabolicabilitiesbutevenintheirmorphologicalappearance,bothat thecellularandcolonylevel.Asanexample,hereisanextractfromtheDuvaland Couret(1912,TulaneUniversity,NewOrleans,Louisiana,USA)publicationonthe experimental production of leprosy in the monkey Macacus rhesus: “The experi- mentalworkservesnotonlytoemphasizethisfact,butisproofthatatransformation fromtheslenderbeadedrodsofthetissuestosolidlystainingdiplococcoidformsof culture does occur for Bacillus leprae; and, conversely, that the coccoid forms of culturemayagainassumetheslenderbeadedappearancebypassagethroughwarm- bloodedanimals.”Advancesinbacterialtransformationstartedtogathermomentum aftertheFrederickGriffithpublicationin1928,althoughthechemicalnatureofthe