Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom.
Department of Biology, Section of Microbiology, University of Copenhagen, Copenhagen, Denmark.
PLoS Genet. 2022 Mar 28;18(3):e1010146. doi: 10.1371/journal.pgen.1010146. eCollection 2022 Mar.
Phage-inducible chromosomal islands (PICIs) are a widespread family of highly mobile genetic elements that disseminate virulence and toxin genes among bacterial populations. Since their life cycle involves induction by helper phages, they are important players in phage evolution and ecology. PICIs can interfere with the lifecycle of their helper phages at different stages resulting frequently in reduced phage production after infection of a PICI-containing strain. Since phage defense systems have been recently shown to be beneficial for the acquisition of exogenous DNA via horizontal gene transfer, we hypothesized that PICIs could provide a similar benefit to their hosts and tested the impact of PICIs in recipient strains on host cell viability, phage propagation and transfer of genetic material. Here we report an important role for PICIs in bacterial evolution by promoting the survival of phage-mediated transductants of chromosomal or plasmid DNA. The presence of PICIs generates favorable conditions for population diversification and the inheritance of genetic material being transferred, such as antibiotic resistance and virulence genes. Our results show that by interfering with phage reproduction, PICIs can protect the bacterial population from phage attack, increasing the overall survival of the bacterial population as well as the transduced cells. Moreover, our results also demonstrate that PICIs reduce the frequency of lysogenization after temperate phage infection, creating a more genetically diverse bacterial population with increased bet-hedging opportunities to adapt to new niches. In summary, our results identify a new role for the PICIs and highlight them as important drivers of bacterial evolution.
噬菌体诱导的染色体岛 (PICI) 是一类广泛存在的高度可移动遗传元件,它们在细菌种群中传播毒力和毒素基因。由于它们的生命周期涉及到辅助噬菌体的诱导,因此它们是噬菌体进化和生态学的重要参与者。PICI 可以在不同阶段干扰其辅助噬菌体的生命周期,导致感染含有 PICI 的菌株后噬菌体产量减少。由于最近发现噬菌体防御系统通过水平基因转移有利于获得外源 DNA,我们假设 PICIs 可以为其宿主提供类似的益处,并测试 PICIs 在受体菌株中对宿主细胞活力、噬菌体繁殖和遗传物质转移的影响。在这里,我们通过促进染色体或质粒 DNA 的噬菌体介导转导转化体的存活,报告了 PICIs 在细菌进化中的重要作用。PICI 的存在为种群多样化和遗传物质的遗传创造了有利条件,例如抗生素抗性和毒力基因。我们的结果表明,通过干扰噬菌体繁殖,PICI 可以保护细菌种群免受噬菌体攻击,从而提高细菌种群和转导细胞的整体存活率。此外,我们的结果还表明,PICI 减少了温和噬菌体感染后的溶原化频率,创造了一个遗传多样性更高的细菌种群,增加了适应新生态位的 bet-hedging 机会。总之,我们的结果确定了 PICIs 的新作用,并强调了它们是细菌进化的重要驱动因素。