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Evolution of Adaptive Immunity from Transposable Nature Reviews Genetics | AOP, published online 9 December 2014; doi:10.1038/nrg3859 PERSPECTIVES independent occasions via recruitment of OPINION non-homologous endonucleases. Owing to the ubiquity and high abun- Evolution of adaptive immunity from dance of MGEs, their co-evolution with cellular hosts is a perennial parasite–host transposable elements combined ‘arms race’ in which the two sides evolved extremely diverse and elaborate systems of defence and counter-defence18–22. Notably, with innate immune systems many defence systems — including restric- tion–modification enzymatic modules, Eugene V. Koonin and Mart Krupovic toxin–antitoxin and the clustered regularly interspaced short palindromic repeat– Abstract | Adaptive immune systems in prokaryotes and animals give rise to CRISPR-associated protein (CRISPR–Cas) long-term memory through modification of specific genomic loci, such as by systems in prokaryotes, and the apop- insertion of foreign (viral or plasmid) DNA fragments into clustered regularly tosis machinery in eukaryotes — seem interspaced short palindromic repeat (CRISPR) loci in prokaryotes and by V(D)J to be ‘guns for hire’; that is, they are also recombination of immunoglobulin genes in vertebrates. Strikingly, recombinases recruited by viruses and other MGEs for counter-defence23,24. derived from unrelated mobile genetic elements have essential roles in both All organisms have a plethora of innate prokaryotic and vertebrate adaptive immune systems. Mobile elements, which immunity mechanisms, and many also have are ubiquitous in cellular life forms, provide the only known, naturally evolved adaptive immunity25–27. In general, innate tools for genome engineering that are successfully adopted by both innate immunity covers all systems of defence immune systems and genome-editing technologies. In this Opinion article, we against a broad range of pathogens, whereas present a general scenario for the origin of adaptive immunity from mobile adaptive immunity is tailored towards a specific pathogen, and its essential feature elements and innate immune systems. is immunological memory, whereby an organism that survives an encounter with a All cellular organisms persist and evolve in the host genome via the ‘cut-and-paste’ particular pathogen is specifically protected under a perennial onslaught of mobile mechanism, whereby the transposon from that pathogen for the long term (often genetic elements (MGEs), such as transpo- is excised from its initial location and for the lifetime of the individual). Adaptive sons, viral sequences and plasmids. Many, if inserted into a new locus. Most of the class II immunity is highly specific and extremely not most, of these diverse, ‘selfish’ elements transposons have characteristic terminal efficient against many pathogens, despite insert into the chromosomes of the cellular inverted repeats (TIRs) but differ widely numerous powerful counter-defence hosts, either as an obligate part of their life with respect to the element size and gene strategies evolved by the pathogens18–22. cycles or at least sporadically. In multicellular content, the mechanisms of transposition In prokaryotes, innate immunity eukaryotes, MGEs constitute a substantial and the transposases encoded8,10,11. The mechanisms include the well-studied proportion of the host genome, for example, majority of the transposases belong to restriction–modification enzymatic modules >50% of the genome in mammals and >70% the DDE superfamily (which is named after and multiple less thoroughly characterized of the genome in some plants1–3. Integrated two aspartate residues and one glutamate systems28. Notable among the latter is the MGEs are also present in the genomes of residue that form the catalytic triad), but recently described mechanism that uses most bacteria and archaea4,5; although they several other unrelated families of trans- bacterial homologues of the eukaryotic are not as abundant as those in eukaryotes, posases have been identified8,10,11. Some Argonaute proteins — the key enzymes of these elements account for up to 30% of some transposons encode transposases that are RNA interference (RNAi) — to generate bacterial genomes6,7. homologous to the rolling-circle replication guide RNA or DNA molecules that are then Transposons are DNA segments that initiation endonucleases found in single- used to inactivate foreign genomes29–31. Until move from one location in the host genome stranded DNA viruses and plasmids12–14, recently, prokaryotes have not been thought to another. Most of the transposons can be whereas other transposases are homologous to have adaptive immunity. However, this grouped into two classes8,9. Class I elements to bacteriophage tyrosine or serine recom- perception was overturned by the discovery (also known as retrotransposons) trans- binases15,16, or to eukaryotic APE1‑like DNA of the CRISPR–Cas systems that are repre- pose via an RNA intermediate which, prior repair endonucleases (which function in con- sented in most archaea and many to integration, is copied back to the DNA junction with reverse transcriptases)17. Such bacteria (FIG. 1a). CRISPR–Cas is an immu- form by the element-encoded reverse trans­ diversity of transposases strongly suggests nity mechanism that functions by incorpo- criptase. Class II DNA transposons move that transposons have emerged on multiple rating fragments of foreign (viral or plasmid) NATURE REVIEWS | GENETICS ADVANCE ONLINE PUBLICATION | 1 © 2014 Macmillan Publishers Limited. All rights reserved PERSPECTIVES a Adaptation cas genes Repeats Spacers Leader Cas1–Cas2 Viral DNA Integration of new protospacer Transcription Expression Transcript processing by Cas nucleases Interference crRNA Cleavage of invading DNA or RNA b Germline configuration V segments D segments J segments Constant region V1 V2 V3 V4 D1 D2 D3 D4 J1 J2 J3 C1 C2 C3 23-RSS 12-RSS RAG1–RAG2 D3 D-to-J recombination J2 V1 V2 V3 V4 D1 D2 J3 C1 C2 C3 + DJ coding Signal joint D4 joint RAG1–RAG2 J1 V-to-DJ recombination D1 V1 V2 V3 D2 J3 C1 C2 C3 + V4 VDJ coding joint Signal joint Transcription and splicing AAA Translation and assembly Variable region Figure 1 | Adaptive immune systems of prokaryotes and eukary- variable region of the immunoglobulin heavy chain is assembled by V(D)J otes. a | The prokaryotic clustered regularly interspaced short palindromic recombination from V (variable; purple rectangle),Nature D (diversity; Reviews green| Genetics rec- repeat–CRISPR-associated protein (CRISPR–Cas) locus consists of cas tangle) and J (joining; brown rectangle) gene segments. The immunoglobu- genes (blue arrows) that encode different Cas proteins, and CRISPR arrays lin light chain is assembled from V and J segments by VJ recombination (not composed of variable spacers (coloured hexagons) interspersed with direct shown). Multiple V, D, J and C (constant region; red rectangles) gene seg- repeats (red triangles). The leader sequence (grey rectangle) contains a pro- ments are available for recombination in the germline genome. The recom- moter for the transcription of the CRISPR array and marks the end where bination is carried out by the RAG1–RAG2 recombinase complex and new spacers are incorporated. Three stages of CRISPR–Cas immunity are involves two types of recombination signal sequences (RSSs), 23‑RSS (red depicted. During the adaptation stage, a Cas1–Cas2 heterohexamer triangles) and 12‑RSS (pink triangles), which flank each gene segment. uptakes a protospacer from the invading plasmid or viral DNA (green) and Joining of the DNA ends requires non-homologous end-joining (NHEJ) pro- incorporates it at the leader-proximal end of the CRISPR array. During the teins (not shown). Two rounds of recombination, D to J and V to DJ, produce expression stage, the CRISPR array is transcribed, and the transcript is pro- a VDJ coding joint and two circular molecules (signal joints); the latter do cessed into small CRISPR RNAs (crRNAs) by different Cas nucleases in a not have any further role and are discarded. Transcription across the VDJ CRISPR–Cas type-dependent manner. During the interference stage, coding joint, followed by splicing, produces the mature transcript of the crRNAs act as guides for the cleavage of invading viral or plasmid DNA or immunoglobulin heavy chain. Subsequent translation of the transcript, RNA that contains regions complementary to the crRNA. b | Lymphocyte assembly of the heavy chain and association with the light chain (beige antigen receptor diversification by V(D)J recombination is shown. The rectangles) complete the assembly of the immunoglobulin receptor. 2 | ADVANCE ONLINE PUBLICATION www.nature.com/reviews/genetics © 2014 Macmillan Publishers Limited. All rights reserved PERSPECTIVES Type I Type II Type III Type IV Cas1 Cas2 Cas1 Cas2 Cas1 Cas2 Adaptation Spacer acquisition and potential Cas4 Cas4 involvement in programmed cell death Cas6 RNase III Cas9 Cas6 Expression Transcript cleavage Cas8 (LS) SS Cas10 (LS) SS Cas8 (LS) SS Interference Cascade complex: crRNA and Cas7 Cas5 Cas9 Cas7 Cas5 Cas7 Cas5 target binding HD-Cas3 Cas3 HD-Cas10 Target cleavage Optional components (function unclear) Csn2 COG1517 DinG Figure 2 | A general scheme of the organization of CRISPR–Cas binding and target cleavage. Similarly, in TypeNature I and Type Reviews III CRISPR–Cas | Genetics systems. Protein names follow the current nomenclature and classifi- systems, Cas6 is a subunit of the Cascade (CRISPR-associated complex cation32. The general functions and the stages of the clustered regularly
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