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Evolution of adaptive immunity from transposable elements combined with innate immune systems

Abstract

Adaptive immune systems in prokaryotes and animals give rise to long-term memory through modification of specific genomic loci, such as by insertion of foreign (viral or plasmid) DNA fragments into clustered regularly interspaced short palindromic repeat (CRISPR) loci in prokaryotes and by V(D)J recombination of immunoglobulin genes in vertebrates. Strikingly, recombinases derived from unrelated mobile genetic elements have essential roles in both prokaryotic and vertebrate adaptive immune systems. Mobile elements, which are ubiquitous in cellular life forms, provide the only known, naturally evolved tools for genome engineering that are successfully adopted by both innate immune systems and genome-editing technologies. In this Opinion article, we present a general scenario for the origin of adaptive immunity from mobile elements and innate immune systems.

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Figure 1: Adaptive immune systems of prokaryotes and eukaryotes.
Figure 2: A general scheme of the organization of CRISPR–Cas systems.
Figure 3: A scenario for the evolution of the CRISPR–Cas system from a casposon, a toxin–antitoxin module and a solo-Cascade innate immune system.
Figure 4: Comparison between TIR, CRISPR and RSS.
Figure 5: Comparison of the proposed evolutionary paths to the prokaryotic and eukaryotic versions of adaptive immunity.

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Acknowledgements

The authors thank K. Makarova for critical reading of the manuscript and comments. E.V.K is supported by intramural funds of the US Department of Health and Human Services (to the National Library of Medicine).

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Koonin, E., Krupovic, M. Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat Rev Genet 16, 184–192 (2015). https://doi.org/10.1038/nrg3859

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