Evolution of RNA- and DNA-guided antivirus defense systems in prokaryotes and eukaryotes: common ancestry vs convergence - PubMed (original) (raw)

Review

Evolution of RNA- and DNA-guided antivirus defense systems in prokaryotes and eukaryotes: common ancestry vs convergence

Eugene V Koonin. Biol Direct. 2017.

Abstract

Complementarity between nucleic acid molecules is central to biological information transfer processes. Apart from the basal processes of replication, transcription and translation, complementarity is also employed by multiple defense and regulatory systems. All cellular life forms possess defense systems against viruses and mobile genetic elements, and in most of them some of the defense mechanisms involve small guide RNAs or DNAs that recognize parasite genomes and trigger their inactivation. The nucleic acid-guided defense systems include prokaryotic Argonaute (pAgo)-centered innate immunity and CRISPR-Cas adaptive immunity as well as diverse branches of RNA interference (RNAi) in eukaryotes. The archaeal pAgo machinery is the direct ancestor of eukaryotic RNAi that, however, acquired additional components, such as Dicer, and enormously diversified through multiple duplications. In contrast, eukaryotes lack any heritage of the CRISPR-Cas systems, conceivably, due to the cellular toxicity of some Cas proteins that would get activated as a result of operon disruption in eukaryotes. The adaptive immunity function in eukaryotes is taken over partly by the PIWI RNA branch of RNAi and partly by protein-based immunity. In this review, I briefly discuss the interplay between homology and analogy in the evolution of RNA- and DNA-guided immunity, and attempt to formulate some general evolutionary principles for this ancient class of defense systems.

Reviewers: This article was reviewed by Mikhail Gelfand and Bojan Zagrovic.

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Figures

Fig. 1

Fig. 1

The evolutionary history of eukaryotic RNAi: assembly from diverse archaeal and bacterial ancestors. The “bacterial” and “archaeal” components of the RNAi protein machinery are assumed to have evolved from the proto-mitochondrial endosymbiont and its archaeal host, respectively. This scenario rests on the fact that RNase III is a protein that is nearly ubiquitous in bacteria but rare in archaea, and the (DNA-dependent) RNA polymerase that is thought to be the ancestor of the RNAi RdRp so far has been identified only in bacteriophages (not in archaeal viruses). However, it cannot be ruled out that these genes have been acquired by the mesophilic archaeal ancestor of eukaryotes (presumably, a member of the Lokiarchaeota) prior to endosymbiosis. RIII, RNAse III

Fig. 2

Fig. 2

The fates of prokaryotic defense systems in eukaryotes. C, CRISPR-Cas; RM, restriction-modification; TA, toxins-antitoxins

Fig. 3

Fig. 3

Evolution of RNA/DNA-guided defense and regulatory systems: from the RNA world to the present

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References

    1. Schroedinger E. What Is Life? with “Mind and Matter” and “Autobiographical Sketches”. Cambridge: Cambridge University Press; 2012.
    1. Crick F. Central dogma of molecular biology. Nature. 1970;227(5258):561–563. doi: 10.1038/227561a0. - DOI - PubMed
    1. Koonin EV. Why the Central Dogma: on the nature of the great biological exclusion principle. Biol Direct. 2015;10:52. doi: 10.1186/s13062-015-0084-3. - DOI - PMC - PubMed
    1. Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971;58(10):465–523. doi: 10.1007/BF00623322. - DOI - PubMed
    1. Koonin EV. The Logic of Chance: The Nature and Origin of Biological Evolution. Upper Saddle River, NJ: FT press; 2011.

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