Abstract
The arms race between cellular life forms and viruses is a major driving force of evolution. A substantial fraction of bacterial and archaeal genomes is dedicated to antivirus defense. We analyzed the distribution of defense genes and typical mobilome components (such as viral and transposon genes) in bacterial and archaeal genomes and demonstrated statistically significant clustering of antivirus defense systems and mobile genes and elements in genomic islands. The defense islands are enriched in putative operons and contain numerous overrepresented gene families. A detailed sequence analysis of the proteins encoded by genes in these families shows that many of them are diverged variants of known defense system components, whereas others show features, such as characteristic operonic organization, that are suggestive of novel defense systems. Thus, genomic islands provide abundant material for the experimental study of bacterial and archaeal antivirus defense. Except for the CRISPR-Cas systems, different classes of defense systems, in particular toxin-antitoxin and restriction-modification systems, show nonrandom clustering in defense islands. It remains unclear to what extent these associations reflect functional cooperation between different defense systems and to what extent the islands are genomic "sinks" that accumulate diverse nonessential genes, particularly those acquired via horizontal gene transfer. The characteristics of defense islands resemble those of mobilome islands. Defense and mobilome genes are nonrandomly associated in islands, suggesting nonadaptive evolution of the islands via a preferential attachment-like mechanism underpinned by the addictive properties of defense systems such as toxins-antitoxins and an important role of horizontal mobility in the evolution of these islands.
Highlights
The arms race between cellular life forms and viruses is a major driving force of evolution
The major mechanisms of defense system variability fueled by the virus-host arms race include rapid sequence evolution, extensive gene duplication, and horizontal gene transfer (HGT), which is often mediated by plasmids carrying the respective defense genes [14, 23, 27, 43, 89]
Statistical analysis of the clustering of defense genes in bacterial and archaeal genomes was performed with 136 clusters of orthologous groups (COGs) in the initial positive set and 3,061 COGs in the initial negative set
Summary
The arms race between cellular life forms and viruses is a major driving force of evolution. The antivirus defense systems function on one of the two general principles, (i) self-nonself discrimination, whereby a defense mechanism recognizes and destroys foreign (e.g., viral) genomes whereas the host genome is protected, and (ii) programmed cell suicide or dormancy induced by infection [48]. Another type of defense machinery that is based on self-nonself discrimination is represented by the CRISPR (clustered regularly interspaced short palindromic repeats)-Cas (CRISPR-associated genes) systems that are encoded in the genomes of the great majority of archaea and many bacteria [31, 38, 54, 88]. It should be noted that defense systems that employ the self-nonself discrimination mechanism have the potential to evolve into systems causing cell suicide or dormancy, as shown for RM systems [22, 33]
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