Evolutionary Genomics of Defense Systems in Archaea and Bacteria

Abstract

Evolution of bacteria and archaea involves an incessant arms race against an enormous diversity of genetic parasites. Accordingly, a substantial fraction of the genes in most bacteria and archaea are dedicated to antiparasite defense. The functions of these defense systems follow several distinct strategies, including innate immunity; adaptive immunity; and dormancy induction, or programmed cell death. Recent comparative genomic studies taking advantage of the expanding database of microbial genomes and metagenomes, combined with direct experiments, resulted in the discovery of several previously unknown defense systems, including innate immunity centered on Argonaute proteins, bacteriophage exclusion, and new types of CRISPR-Cas systems of adaptive immunity. Some general principles of function and evolution of defense systems are starting to crystallize, in particular, extensive gain and loss of defense genes during the evolution of prokaryotes; formation of genomic defense islands; evolutionary connections between mobile genetic elements and defense, whereby genes of mobile elements are repeatedly recruited for defense functions; the partially selfish and addictive behavior of the defense systems; and coupling between immunity and dormancy induction/programmed cell death.

Keywords: CRISPR-Cas; adaptive immunity; antivirus defense; dormancy; innate immunity; mobile genetic elements; programmed cell death; restriction-modification; toxins-antitoxins.

Figure 1

Abundance of the major types of defense systems in bacterial and archaeal genomes. Smoothed probability density for the distributions across 4,961 complete genomes of bacteria and archaea is shown. The number of genes in each category was calculated as described earlier (109). Abbreviations: ABI, abortive infection; CRISPR, clustered regularly interspaced short palindromic repeats; RM, restriction modification; TA, toxin-antitoxin.

Figure 2

Scaling of the major types of defense systems with the total number of genes. Tan data points represent the total abundance of the respective defense systems in individual genomes; lines show the power law scaling relative to the genome size. The number of genes in each category and the power law scaling parameters were calculated as described earlier (109). Abbreviations: ABI, abortive infection; CRISPR, clustered regularly interspaced short palindromic repeats; RM, restriction modification; TA, toxin-antitoxin.

Figure 3

Principal component analysis of bacterial and archaeal defense systems (abortive infection, CRISPR, restriction modification, toxin-antitoxin). Excess or deficit (in natural log scale) of the five groups of defense systems relative to the expectations, derived from the genome size, was projected into the space of the first two principal components, as described previously (109).

Figure 4

Length distributions of defense islands in bacterial and archaeal genomes.

Figure 5

Defense islands as a potential source of novel defense systems. For each island, the genome name, the respective nucleotide sequence ID, and genomic coordinates are provided. Block arrows indicate the direction of tAranscription, roughly to scale. PIN, HNH, and PD-D/ExK are distinct nuclease families. Abbreviations: HTH, helix-turn-helix; HTH-MP, HTH domain fused to Zn-dependent metalloprotease.