CRISPR-Cas Systems: RNA-mediated Adaptive Immunity in Bacteria and Archaea

299 Pages·2013·7.45 MB·English

by  Francisco J. M. Mojica

CRISPR-Cas Systems
Rodolphe Barrangou John van der Oost
•
Editors
CRISPR-Cas Systems
RNA-Mediated Adaptive Immunity
in Bacteria and Archaea
123
Editors
Rodolphe Barrangou Johnvan derOost
DuPontNutritionand Health Laboratory ofMicrobiology
Madison, WI Wageningen University
USA Wageningen
The Netherlands
ISBN 978-3-642-34656-9 ISBN 978-3-642-34657-6 (eBook)
DOI 10.1007/978-3-642-34657-6
SpringerHeidelbergNewYorkDordrechtLondon
LibraryofCongressControlNumber:2012953370
(cid:2)Springer-VerlagBerlinHeidelberg2013
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We dedicate this book to the CRISPR
community—past, present and future
Preface
Clusteredregularlyinterspacedshortpalindromicrepeats(CRISPR),togetherwith
associatedsequences(casgenesandCasproteins)formtheCRISPR-Casadaptive
immune system, which is present in most archaea and many bacteria. This rela-
tivelynovel familyofrepeats wasfirstdiscovered in1987,characterizedin2002,
implicatedinimmunityin2005,andshowntoprovideacquiredresistanceagainst
bacterial viruses in 2007. Since, it has been implicated in providing adaptive
immunity against bacteriophages, archaeal viruses, and plasmids in numerous
organisms.Thedevelopmentofseveralfunctionalmodelsystemsintherecentpast
has paved the way for thorough scientific investigations of these unique and
intriguing defense systems.
Notwithstandingextensivesequencediversityandgenecontentpolymorphism,
CRISPR-Cas systems have recently been categorized into three types, based on
phylogenyandmolecularmechanismofaction.Thishassetthestageforarevision
of the nomenclature, and collective agreement on terminology, representation
standards, and definition of the various stages that render CRISPR-mediated
immunity. Mechanistically, CRISPR-Cas systems drive immunity through three
majorsteps:(1)acquisition,whereimmunizationoccursbyuptakeofforeignDNA
sequence and integration as new CRISPR spacers; (2) expression, where Cas
proteins are produced and CRISPR-encoded transcripts are processed into small
interfering CRISPR RNAs (crRNAs); (3) interference, where crRNA-Cas
ribonucleoprotein complexes mediate homologous target recognition and specific
cleavage. The ability of this idiosyncratic system to integrate short DNA
sequences from invasive elements into the chromosome renders adaptive immu-
nity inheritable.
This book provides a unique perspective into the historical events and key
discoveriesthathaveunraveledthefunctionsofCRISPR-Cassystemsandtheroles
they play in bacterial and archaeal biology and evolution. Once the occurrence,
diversity, function, and evolution of CRISPR are established, each CRISPR-Cas
type is specifically characterized. Their roles in various biological processes (not
restrictedtodefense)arediscussed,andapplicationsareoutlined.Theirimpacton
vii
viii Preface
microbial populations and evolutions are outlined, thus setting the stage for a
deeperunderstandingof CRISPR-Cas systems.
Although there are mechanistic commonalities between CRISPR-mediated
immunity and RNAi, notably small non-coding RNA-mediated cleavage of
complementary target nucleic acid sequences (generally DNA, but one sub-type
eliminates RNA) by a ribonucleoprotein complex, there are fundamental
differences in the molecular processes that drive these two phenomena. Function-
ally, in addition to providing adaptive immunity against exogenous viral and
plasmid dsDNA, at least some CRISPR-Cas systems appear to play a role in
host-regulatory processes. Several applications have been established, notably
build up of phage resistance, and exploiting hypervariability for typing and
epidemiological surveys. Moreover, the ability to re-program the cleavage
machinery has opened new avenues for customized DNA restriction, nicking,
genomeengineering and editing.
SomeofthecontributorshavebeenintimatedwithCRISPRsequencesformany
years, and provided their personal perspective on this fast-evolving and exciting
field. Likewise, several authors have been very active members of the CRISPR
researchcommunityandhavehadtheprivilegetoparticipateintheannualCRISPR
meetingshostedatUCBerkeleysince2008,andatWageningenUniversityin2010.
The material presented here illustrates the frenetic pace at which the field has
evolved over the last five years, and the breadth and scope of topics discussed
reflectthescientificallydiversecommunitywhichhascometogether,coveringfoci
including molecular studies, genetic analyses, mathematical modeling, evolution,
functionalimplementation,epidemiology,metagenomics,andecology.Thevariety
ofentrywaysintothefield,anddiversityofthevantagepointsofthevariousgroups
involvedillustratestherelevanceofthetopic.CurrentimplementationofCRISPR-
Cassystemstodevelopphageresistanceindairystartercultureshasalreadyshown
that CRISPR can be leveraged industrially. Current analyses of CRISPR
polymorphisminpathogenicspecieswilldeterminehowrelevanttheselocimaybe
for epidemiological surveys, clinical analyses, andfood safety.
We would like to acknowledge all the authors, our colleagues, collaborators,
and CRISPR meeting participants for all their contributions to the field, colorful
opinions, and insightful conversations.
Looking back, the significant advances in studying the CRISPR mechanism of
actionhavesetthestageforapplicationsandareasofinvestigation,andestablisha
solid basis for future studies that will investigate the outstanding mysteries and
questions that remain unanswered. We are hopeful that the need for proper
bioinformatics tools will be addressed, and that NCBI will integrate CRISPR-
related resources. Doubtless, we predict that the community camaraderie and
scientific diversity will pave the way for a bright future of CRISPR as a field.
Certainly, the visibility of the field as measured by ever-increasing quantity,
spectacular quality, and impressive citation rates of CRISPR-related publications
warrant a bright future. This may just be the beginning…
Contents
1 Discovery and Seminal Developments in the CRISPR Field . . . . . 1
Francisco J. M. Mojica and Roger A. Garrett
2 Occurrence, Diversity of CRISPR-Cas Systems
and Genotyping Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
Christine Pourcel and Christine Drevet
3 Evolution and Classification of CRISPR-Cas Systems
and Cas Protein Families . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
Kira S. Makarova and Eugene V. Koonin
4 Regulation of CRISPR-Based Immune Responses . . . . . . . . . . . . 93
Zihni Arslan, Edze R. Westra, Rolf Wagner and Ümit Pul
5 crRNA Biogenesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115
Emmanuelle Charpentier, John van der Oost
and Malcolm F. White
6 Distribution and Mechanism of the Type I
CRISPR-Cas Systems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
Raymond H. J. Staals and Stan J. J. Brouns
7 Type II: Streptococcus thermophilus . . . . . . . . . . . . . . . . . . . . . . 171
Marie-Ève Dupuis and Sylvain Moineau
8 Type III CRISPR-Cas Systems and the Roles
of CRISPR-Cas in Bacterial Virulence . . . . . . . . . . . . . . . . . . . . 201
Asma Hatoum-Aslan, Kelli L. Palmer, Michael S. Gilmore
and Luciano A. Marraffini
ix
x Contents
9 CRISPR-Cas Systems to Probe Ecological Diversity
and Host–Viral Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
Nicole L. Held, Lauren M. Childs, Michelle Davison,
Joshua S. Weitz, Rachel J. Whitaker and Devaki Bhaya
10 Roles of CRISPR in Regulation of Physiological Processes. . . . . . 251
Gil Amitai and Rotem Sorek
11 Applications of the Versatile CRISPR-Cas Systems . . . . . . . . . . . 267
Philippe Horvath, Giedrius Gasiunas, Virginijus Siksnys
and Rodolphe Barrangou
12 CRISPRs in the Microbial Community Context. . . . . . . . . . . . . . 287
Jillian F. Banfield
Glossary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297
Chapter 1
Discovery and Seminal Developments
in the CRISPR Field
Francisco J. M. Mojica and Roger A. Garrett
Abstract Inthelate1980sandearly1990s,arraysofregularlyspacedrepeatswere
detected in both bacterial and archaeal genomes. They are currently known as
ClusteredRegularlyInterspacedShortPalindromicRepeatsorCRISPR.Advances
in our understanding of their biological significance and potential applications
for biotechnology have followed a two-phased development. Initial studies were
few and mainly descriptive of arrays of interspaced repeats in bacteria and
archaea and of physically linked conserved genes that were inferred to be co-
functional. Moreover, before their function was revealed, repeat-spacer arrays of
Mycobacteriumsppwereemployedasnovelmarkersforbacterialgenotyping.The
secondphasebeganin2005,withthediscoveryofalinkbetweenCRISPRarrays
and host protection against invading genetic elements. This finding fuelled a
plethora of biochemical and genetic studies directed at characterising the mecha-
nisticdetailsofthisnovelandcomplexgeneticbarrier.First,thisledtothefinding
thattherepeats,spacers,CRISPR-associated(Cas)proteinsandpartiallyconserved
leader regions flanking one end of the CRISPR array, constitute the essential
functionalcomponents.Subsequently,threeprimaryfunctionalstepsweredefined:
(1)acquisition(alsotermedadaptation):uptakeofnewspacersatorneartheleader
sequence,(2)expression:generationofCRISPRtranscriptsfromwithintheleader
regionandtheirprocessingintosmallmatureCRISPRRNAs(crRNAs)carryingall
or most of the spacer sequence and (3) interference: involving protein-crRNA
F.J.M.Mojica(&)
DepartamentodeFisiología,GenéticayMicrobiología,
UniversidaddeAlicante,03080Alicante,Spain
e-mail:[email protected]
R.A.Garrett
DepartmentofBiologyBiocenter,ArchaeaCentre,
UniversityofCopenhagen,2200NCopenhagen,Denmark
e-mail:[email protected]
R.BarrangouandJ.vanderOost(eds.),CRISPR-CasSystems, 1
DOI:10.1007/978-3-642-34657-6_1,(cid:2)Springer-VerlagBerlinHeidelberg2013
2 F.J.M.MojicaandR.A.Garrett
complexestargetingandcleavingforeigngeneticelements.Onlynowcanwebegin
tocomprehendthecomplexfunctionalinteractionsanddiversityofCRISPR-based
systems,andtheimplicationsoftheiradaptivenature.Here,wedescribetheearly
developmentsintheCRISPRfieldandrelatethemtoourcurrentunderstandingof
how thesenovel,complex and diverse systems function.
Contents
1.1 Introduction....................................................................................................................... 2
1.2 EarlyBreakthroughs......................................................................................................... 4
1.2.1 RegularlySpacedRepeats.................................................................................... 4
1.2.2 DirectRepeatsinMycobacteria........................................................................... 4
1.2.3 TREPsinHaloarchaea.......................................................................................... 5
1.2.4 NewFamilyofProkaryoticRepeats.................................................................... 5
1.2.5 DistributionofCRISPRArraysAmongstArchaeaandBacteria....................... 6
1.2.6 DiscoveryofProcessedCRISPRTranscripts...................................................... 7
1.2.7 IdentificationofCRISPR-associatedProteins..................................................... 8
1.3 CRISPR-CasFunctionRevealed...................................................................................... 10
1.3.1 EarlyHypotheses.................................................................................................. 10
1.3.2 TheLinktoInvadingGeneticElements............................................................. 10
1.3.3 FunctionalDiversityofCRISPRSystems........................................................... 12
1.4 FunctionalComponentsofCRISPR-BasedSystems...................................................... 16
1.4.1 CRISPR-associated(Cas)Proteins....................................................................... 16
1.4.2 CRISPRArrays..................................................................................................... 18
1.4.3 Leaders.................................................................................................................. 19
1.4.4 Repeats.................................................................................................................. 20
1.4.5 Spacers.................................................................................................................. 21
1.4.6 ProtospacerAdjacentMotifs................................................................................ 23
1.4.7 CRISPRRNAs...................................................................................................... 23
1.5 Reflections........................................................................................................................ 25
References.................................................................................................................................. 26
1.1 Introduction
Clusters of regularly interspaced short palindromic repeats (CRISPR) were first
observed in bacteria in the late 1980s and, in the mid-1990s, in the genomes of
various archaeal lineages. Their apparent broad distribution suggested that they
mightplayacommonandfundamentalcellularroleinbotharchaealandbacterial
domains,althoughtheirprevalenceinextremophilicorganismssuggestedthatthey
might in some way facilitate adaptation to extreme environments (Mojica et al.
2000; Jansen et al. 2002a). The [repeat-spacer] arrays were distinct in structure
n
and sequence from other known functional repeat-based systems and