The defense island repertoire of the Escherichia coli pan-genome

PLoS Genet. 2023 Apr 6;19(4):e1010694. doi: 10.1371/journal.pgen.1010694. eCollection 2023 Apr.

Abstract

It has become clear in recent years that anti-phage defense systems cluster non-randomly within bacterial genomes in so-called "defense islands". Despite serving as a valuable tool for the discovery of novel defense systems, the nature and distribution of defense islands themselves remain poorly understood. In this study, we comprehensively mapped the defense system repertoire of >1,300 strains of Escherichia coli, the most widely studied organism for phage-bacteria interactions. We found that defense systems are usually carried on mobile genetic elements including prophages, integrative conjugative elements and transposons, which preferentially integrate at several dozens of dedicated hotspots in the E. coli genome. Each mobile genetic element type has a preferred integration position but can carry a diverse variety of defensive cargo. On average, an E. coli genome has 4.7 hotspots occupied by defense system-containing mobile elements, with some strains possessing up to eight defensively occupied hotspots. Defense systems frequently co-localize with other systems on the same mobile genetic element, in agreement with the observed defense island phenomenon. Our data show that the overwhelming majority of the E. coli pan-immune system is carried on mobile genetic elements, explaining why the immune repertoire varies substantially between different strains of the same species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / genetics
  • Escherichia coli* / genetics
  • Genome, Bacterial* / genetics

Grants and funding

R.S. was supported, in part, by the European Research Council (grant ERC-AdG GA 101018520), Israel Science Foundation (grant ISF 296/21), the Deutsche Forschungsgemeinschaft (SPP 2330, grant 464312965), the Ernest and Bonnie Beutler Research Program of Excellence in Genomic Medicine, the Minerva Foundation with funding from the Federal German Ministry for Education and Research, and the Knell Family Center for Microbiology. D.H. was supported in part by a fellowship from the Israel Ministry of Absorption. A.M. was supported by a fellowship from the Ariane de Rothschild Women Doctoral Program and, in part, by the Israeli Council for Higher Education via the Weizmann Data Science Research Center.