Interactions between mobile genetic elements: An anti-phage gene in an integrative and conjugative element protects host cells from predation by a temperate bacteriophage

Most bacterial genomes contain horizontally acquired and transmissible mobile genetic elements, including temperate bacteriophages and integrative and conjugative elements. Little is known about how these elements interact and co-evolved as parts of their host genomes. In many cases, it is not known what advantages, if any, these elements provide to their bacterial hosts. Most strains of Bacillus subtilis contain the temperate phage SP ss and the integrative and conjugative element ICEBs1. Here we show that the presence of ICEBs1 in cells protects populations of B. subtilis from predation by SP ss, likely providing selective pressure for the maintenance of ICEBs1 in B. subtilis. A single gene in ICEBs1 (yddK, now called spbK for SP ss killing) was both necessary and sufficient for this protection. spbK inhibited production of SP ss, during both activation of a lysogen and following de novo infection. We found that expression spbK, together with the SP ss gene yonE constitutes an abortive infection system that leads to cell death. spbK encodes a TIR (Toll-interleukin-1 receptor)-domain protein with similarity to some plant antiviral proteins and animal innate immune signaling proteins. We postulate that many uncharacterized cargo genes in ICEs may confer selective advantage to cells by protecting against other mobile elements. Author summary Chromosomes from virtually all organisms contain genes that were horizontally acquired. In bacteria, many of the horizontally acquired genes are located in mobile genetic elements, elements that promote their own transfer from one cell to another. These elements include viruses and conjugative elements that are parts of the host genome and they can contain genes involved in metabolism, pathogenesis, symbiosis, and antibiotic resistances. Interactions between these elements are poorly understood. Furthermore, the majority of these elements confer no obvious benefit to host cells. We found that the presence of an integrative and conjugative element (ICE) in a bacterial genome protects host cells from predation by a bacteriophage (virus). There is a single gene in the integrative and conjugative element that confers this protection, and one gene in the bacteriophage that likely works together with the ICE gene. When expressed at the same time, these two genes cause cell death, before functional viruses can be made and released to kill other cells. We postulate that other ICEs may confer selective advantage to their host cells by protecting against other mobile elements.