Nucleic Acids and Molecular Biology 32 Béatrice Clouet-d’Orval Editor RNA Metabolism and Gene Expression in Archaea Nucleic Acids and Molecular Biology Volume 32 Serieseditor AllenW.Nicholson Philadelphia,PA19122,USA Moreinformationaboutthisseriesathttp://www.springer.com/series/881 Be´atrice Clouet-d’Orval Editor RNA Metabolism and Gene Expression in Archaea Editor Be´atriceClouet-d’Orval LaboratoiredeMicrobiologieetdeGe´ne´tique Mole´culaires(LMGM),CentredeBiologieInte´grative(CBI) Universite´deToulouse,CNRS Toulouse,France ISSN0933-1891 ISSN1869-2486 (electronic) NucleicAcidsandMolecularBiology ISBN978-3-319-65794-3 ISBN978-3-319-65795-0 (eBook) DOI10.1007/978-3-319-65795-0 LibraryofCongressControlNumber:2017957625 ©SpringerInternationalPublishingAG2017 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartof the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,broadcasting,reproductiononmicrofilmsorinanyotherphysicalway,andtransmissionor informationstorageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilar methodologynowknownorhereafterdeveloped. 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Printedonacid-freepaper ThisSpringerimprintispublishedbySpringerNature TheregisteredcompanyisSpringerInternationalPublishingAG Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Outline and Synopsis AlthoughmanyreviewsandbookssurveymanyaspectsofRNAinBacteriaandin Eukarya, no book has so far attempted to provide a panoramic view of enzymes, machines,andpathwaysthatsynthetize,modify,anddegradeRNAinArchaea,the thirddomainoflife. The early studies of C.R Woese of microbial phylogeny based on rRNA sequences yielded the remarkable finding that the prokaryotic world was not monophyletic but separated into two distinct domains: Archaea and Bacteria. This major advance during the last part of the twentieth century opened a novel vision of the living world. The universal tree predicted that the Archaea were specific relatives of the Eukarya, to the exclusion of the Bacteria. Astonishingly, geneticinformationprocessingsystemsintheArchaeaareoftencloselyrelatedto theircounterpartsineukaryotes(translation,transcription,replication,DNArecom- bination,andrepair)evenifArchaeahaveabacteria-likecellularstructure.Archaea arenow consideredasmodelswithanemphasisonstudying themolecularmech- anisms that universally conserve the evolutionary history of life and for the emergence of new technologies. With the advent of whole genome sequencing, a promisingwaytotakeadvantageofthesesimilaritiesistoanalyzetheevolutionof cellular systems through phylogenomic approaches. Over the years, our vision of archaeal microorganisms has evolved from exotic microbial extremophiles to organismsofgeneralimportancethatareusedtoelucidatefundamentalbiological questions. More recently, a newly discovered deep-sea archaeon named Loki suggests eukaryotes evolved directly from archaea rather than representing a separate branch of life. In consideration of this fundamental finding, Archaea are now renowned to be important model microorganisms for the study of molecular mechanisms that are conserved between Eukarya and Archaea. In particular, ArchaeaandEukaryasharemanyRNAbiologyaspectswhichareatthecenterof cellularregulationpathways.Majorexamplesarethe3Dstructuresofthearchaeal RNA polymerase and archaeal exosome which resemble eukaryal RNA polymer- asesandRNA-degradingexosomecomplexes,respectively.Moreover,mostofthe archaeal tRNA and rRNA modifications rely on RNP guide machineries orthologoustotheeukaryalC/D andH/ACA RNPcomplexes. Thishighlights the v vi OutlineandSynopsis advantage of an archaeal model to gain further mechanistic and evolutionary information of fundamental processes across the three domains of life. Neverthe- less, for over a decade, numerous signaling pathways have been described in Eukarya and Bacteria in which RNA processing regulates gene expression. In Archaea, these processes have been overlooked. Molecular mechanisms of RNA maturation and decay and posttranscriptional control of gene expression are far fromunderstood. Given that the RNA field is moving very fast, it is time to cover many of the excitingandsometimesoverlookeddevelopmentsinthefieldthatrevealoriginality ofthearchaealsystemandilluminatethefascinatingbiologythatsetsthestagefor RNA. Therefore, this volume of Nucleic Acid and Molecular Biology provides a reviewofourknowledgeondifferentaspectsofRNAbiologyinarchaealcellsfrom synthesistodegradationthroughmodification,maturation,andregulatoryfunction aswellasdefensesystemincludingevolutionaryconsiderationsofthoseprocesses. However,thefieldofarchaealvirologywillnotbediscussedinthisbooksinceto datethereisnoevidenceontheexistenceofarchaealRNAvirusesoranyregulatory RNAmoleculesinvolvedintheviruslifecycles. Thistaskisachievedby11chaptersthatcollectivelysummarizerecentadvances inourunderstandingofRNAmetabolismatalllevels. Contents 1 AGlobalCharacterisationoftheArchaealTranscription Machinery. .. . . . . . .. . . . . . .. . . . . .. . . . . . .. . . . . . .. . . . . .. . 1 KatherineSmollett,FabianBlombach,ThomasFouqueau, andFinnWerner 2 TranscriptionFactor-MediatedGeneRegulationinArchaea. . . . . 27 ElizabethA.Karr,CatherineE.Isom,VyTrinh,andEvelinePeeters 3 TranslationRegulation:TheArchaea-EukaryalConnection. . . . . 71 DarioBenelli,AnnaLaTeana,andPaolaLondei 4 AnOverviewofRibonucleaseRepertoireandRNAProcessing PathwaysinArchaea. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89 DuyKhanhPhung,MarieBouvier,andBe´atriceClouet-d’Orval 5 TheArchaealExosome:DegradationandTailingatthe30-End ofRNA. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115 ElenaEvguenieva-Hackenberg,SusannGauernack,andGabriele Klug 6 LifeandDeathofRibosomesinArchaea. . . . . . . . . . . . . . . . . . . . 129 Se´bastienFerreira-Cerca 7 StructureandFunctionofArchaealRibonucleaseP. . . . . . . . . . . . 159 MakotoKimura,KosukeOshima,XuzhuGao,DanJiang, TakashiNakashima,andToshifumiUeda 8 FunctionandBiosynthesisoftheUniversaltRNAModification N6-Threonylcarbamoyl-Adenosine. . . . . . . . . . . . . . . . . . . . . . . . . 177 AdelinePichard-Kostuch,Marie-ClaireDaugeron,PatrickForterre, andTamaraBasta 9 EvolutionofC/DBoxsRNAs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201 VanessaTrippandLennartRandau vii viii Contents 10 DiverseFunctionsofSmallRNAs(sRNAs)inHalophilicArchaea: FromNon-codingRegulatorysRNAstoMicroprotein-Encoding sRNAs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225 JanaKliemtandJ€orgSoppa 11 CRISPRandSalty:CRISPR-CasSystemsinHaloarchaea. . . . . . . 243 Lisa-KatharinaMaier,OmerS.Alkhnbashi,RolfBackofen, andAnitaMarchfelder Chapter 1 A Global Characterisation of the Archaeal Transcription Machinery KatherineSmollett,FabianBlombach,ThomasFouqueau, andFinnWerner Abstract Archaeaemployaeukaryote-liketranscriptionapparatustotranscribea bacteria-like genome; while the RNA polymerase, basal factors and promoter elements mirror the eukaryotic RNA polymerase II system, archaeal genomes are densely packed with genes organised into multicistronic transcription units. The molecular mechanisms of archaeal transcription have been studied and characterised in great detail in vitro, but until recently relatively little was known about its global characteristics. In this chapter we discuss an integrated view of transcription from the molecular to the global level. Systems biology approaches haveprovidedcompellinginsightsintopromoterandterminatorDNAelements,the genome-wide distribution of transcription initiation- and elongation factors and RNA polymerase, the archaeal transcriptome and chromatinorganisation. Overall theseanalysesilluminatetranscriptionfromagenome-wideperspectiveandserve as a resource for the community. In addition, Big Data can often validate mecha- nistic models based on biochemical and structural information, and generate new workinghypothesesthatcanbethoroughlytestedanddissectedinvitro.Thisisan excitingtimetostudygeneexpressioninthearchaeasinceweareatthebrinkofa comprehensiveyetdetailedunderstandingoftranscription. 1.1 Introduction Archaeaareprokaryotesandassuchsharemanypropertieswithbacteriaincluding circular genomes, densely packed with genes organised into operons. However, their transcription machinery is closely related to that of RNA polymerase II, the enzymeresponsibleformRNAtranscriptionineukaryotes(Fig.1.1).Thissimilar- ity extends from the RNA polymerase (RNAP) subunit composition, via general transcription factors required for initiation, to their cognate promoter elements (Fig. 1.1a, b) (Werner and Grohmann 2011). In essence, archaeal transcription K.Smollett(cid:129)F.Blombach(cid:129)T.Fouqueau(cid:129)F.Werner(*) InstituteofStructuralandMolecularBiology,DivisionofBiosciences,UniversityCollege London,GowerStreet,LondonWC1E6BT,UK e-mail:[email protected] ©SpringerInternationalPublishingAG2017 1 B.Clouet-d’Orval(ed.),RNAMetabolismandGeneExpressioninArchaea, NucleicAcidsandMolecularBiology32,DOI10.1007/978-3-319-65795-0_1