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Evolutionary entanglement of mobile genetic elements and host defence systems: guns for hire

Nature Reviews Genetics volume 21, pages 119–131 (2020)Cite this article

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Abstract

All cellular life forms are afflicted by diverse genetic parasites, including viruses and other types of mobile genetic elements (MGEs), and have evolved multiple, diverse defence systems that protect them from MGE assault via different mechanisms. Here, we provide our perspectives on how recent evidence points to tight evolutionary connections between MGEs and defence systems that reach far beyond the proverbial arms race. Defence systems incur a fitness cost for the hosts; therefore, at least in prokaryotes, horizontal mobility of defence systems, mediated primarily by MGEs, is essential for their persistence. Moreover, defence systems themselves possess certain features of selfish elements. Common components of MGEs, such as site-specific nucleases, are ‘guns for hire’ that can also function as parts of defence mechanisms and are often shuttled between MGEs and defence systems. Thus, evolutionary and molecular factors converge to mould the multifaceted, inextricable connection between MGEs and anti-MGE defence systems.

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Fig. 1: Distribution of mobile genetic elements and defence systems in the virtual space bounded by the axes of selfishness and mobility.
Fig. 2: Competition between mobile genetic elements as a host defence strategy.
Fig. 3: Domestication of transposases and integrases for ‘natural genome engineering’.
Fig. 4: Guns for hire: shuttling of components between MGEs and cellular organisms.

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Acknowledgements

E.V.K. thanks U. Gophna (Tel Aviv University) and E. Westra (University of Exeter) for inspiring discussions. E.V.K., K.S.M. and Y.I.W. are supported by the Intramural Research Program funds of the US National Institutes of Health (US Department of Health and Human Services). M.K. was supported by the Agence Nationale de la Recherche (France) project ENVIRA (no. ANR-17-CE15-0005-01).

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  1. National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD, USA

    Eugene V. Koonin, Kira S. Makarova & Yuri I. Wolf

  2. Department of Microbiology, Institut Pasteur, Paris, France

    Mart Krupovic

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E.V.K. and M.K. wrote the manuscript. All authors researched data for the article and contributed to discussion of the content and reviewing/editing of the manuscript before submission.

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Glossary

Abortive infection systems

Toxin–antitoxin systems that abrogate virus infection by inducing cell dormancy or death.

Autoimmunity

Immune reaction to self (that is, components of the organism itself instead of components of mobile genetic elements). Autoimmunity stems from failure of self versus non-self discrimination mechanisms.

CRISPR–Cas

Prokaryotic adaptive immunity systems that create an immune memory bank by integrating fragments of foreign genomes into CRISPR arrays and use them to recognize and inactivate the cognate foreign nucleic acid.

Exapted

Pertaining to exaptation, which is recruitment of a biological feature for a function that is different from the function it had been selected for.

Horizontal gene transfer

(HGT). Transfer of genes between organisms by any means other than vertical transmission from parents to offspring.

Integrative conjugative elements

(ICEs). A diverse class of mobile genetic elements present in numerous bacteria that are integrated into bacterial chromosomes and are inherited vertically but retain the capacity to excise and move horizontally by conjugation.

Lytic viruses

Viruses that, at the end of their reproduction cycle, lyse and kill the infected cell.

Mobile genetic elements

(MGEs). Genetic elements that are prone to changing locations within the same genome (e.g. transposons) or to horizontal transfer between host cells (e.g. viruses and plasmids). Many MGEs encompass genes mediating self-replication.

Restriction–modification systems

(RM systems). A variety of prokaryotic defence systems that contain distinct modification components (typically DNA methyltransferases) that modify and thus protect the self DNA, and restriction endonucleases that cleave unmodified, foreign DNA.

Temperate viruses

Viruses that integrate into the host genome, forming proviruses, but retain the capacity of induction followed by a lytic cycle.

Toxin–antitoxin modules

(TA modules). Genetic elements that consist of a toxin component (often a nuclease) and an antitoxin component that binds and transiently inactivates the toxin. When the antitoxin is inactivated, typically under stress, the toxin induces cell dormancy or death.

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Koonin, E.V., Makarova, K.S., Wolf, Y.I. et al. Evolutionary entanglement of mobile genetic elements and host defence systems: guns for hire. Nat Rev Genet 21, 119–131 (2020). https://doi.org/10.1038/s41576-019-0172-9

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