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

• Published in: Nature reviews. Genetics Vol. 21; no. 2; pp. 119 - 131
• Main Authors: Koonin, Eugene V., Makarova, Kira S., Wolf, Yuri I., Krupovic, Mart
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.02.2020; Nature Publishing Group
• Subjects: 631/181/2474; 631/181/735; 631/208/212/2305; 631/208/4041; 631/208/726/2001/1428; 631/326/596/2554; Agriculture; Animal Genetics and Genomics; Biological Evolution; Biomedical and Life Sciences; Biomedicine; Cancer Research; Cooling; CRISPR; Defense mechanisms; Evolution; Evolution, Molecular; Evolutionary genetics; Gene Function; Gene Transfer, Horizontal; Genetic aspects; Genetic diversity; Genetic research; Host-parasite interactions; Host-Pathogen Interactions; Host-virus relationships; Human Genetics; Interspersed Repetitive Sequences; Life Sciences; Military markets; Military sales; Mobility; Nuclease; Perspective; Prokaryotes; United States; Molecular evolution; Evolutionary genetics; DNA transposable elements; Viral evolution; Mobile elements; CRISPR-Cas systems
• ISSN: 1471-0056; 1471-0064; 1471-0064
• DOI: 10.1038/s41576-019-0172-9

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. Incessant encounters of all cellular life forms with mobile genetic elements (MGEs) have driven the evolution of diverse defence mechanisms, including CRISPR–Cas and restriction–modification systems. In this Perspective, Koonin, Makarova, Wolf and Krupovic describe the surprisingly intricate interplay between MGEs and host defence systems. Not only do defence systems commonly show high horizontal mobility but many molecular components are ‘guns for hire’ that have been co-opted by defence systems from MGEs and vice versa.