Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis.

Phage-inducible chromosomal islands promote genetic variability by blocking phage reproduction and protecting transductants from phage lysis.
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DOI:
10.1371/journal.pgen.1010146
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发表时间:
2022-03
期刊:
影响因子:
4.5
通讯作者:
Haag AF
Haag AF
中科院分区:
生物学2区
文献类型:
--
作者:
Ibarra-Chávez R;Brady A;Chen J;Penadés JR;Haag AF

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噬菌体诱导染色体岛(PICIs)是一个广泛存在的高移动遗传元件家族,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。由于噬菌体防御系统最近被证明有利于通过水平基因转移获得外源DNA,我们假设pici可以为其宿主提供类似的益处,并测试了pici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,我们报道了PICIs在细菌进化中的重要作用,通过促进噬菌体介导的染色体或质粒DNA转导剂的存活。pici的存在为种群多样化和转移的遗传物质(如抗生素抗性和毒力基因)的遗传创造了有利条件。我们的研究结果表明,通过干扰噬菌体的繁殖,PICIs可以保护细菌群体免受噬菌体的攻击,提高细菌群体和转导细胞的总体存活率。此外,我们的研究结果还表明,pici减少了温带噬菌体感染后溶原的频率,创造了一个更具遗传多样性的细菌群体,增加了适应新生态位的下注对冲机会。总之,我们的研究结果确定了pici的新作用,并强调它们是细菌进化的重要驱动因素。细菌需要保护自己免受噬菌体的感染和杀死,才能在环境中生存。为此,细菌已经发展出一套复杂的防御机制,可以保护单个细胞或整个细菌群。个体化保护是通过CRISPR-Cas或溶原化等系统实现的,这些系统允许受感染的细胞存活。相比之下,基于群体的保护,如流产感染系统,在噬菌体后代被释放之前导致细胞死亡。在这里,我们描述了噬菌体诱导的染色体岛(PICIs)在保护细菌群体免受噬菌体捕食方面的新作用。由此产生的存活率的提高对猎物群体获得外来DNA(如抗菌素耐药性和适应性基因)产生了影响,因为它也允许获得新遗传物质的细菌的存活率增加。作为增加存活率的直接结果,pici扩大了细菌种群的遗传多样性。这种增加的遗传多样性对整个细菌种群是有利的,因为在任何给定的环境中,适应性最好的克隆都将胜过其他克隆。因此,pici也是人口多样化的关键中介。
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. Bacteria need to protect themselves from infection and killing by phages to survive in the environment. For this purpose, bacteria have developed a sophisticated arsenal of defense mechanisms that can protect individual cells or the overall bacterial population. Individualized protection is achieved via systems such as CRISPR-Cas or lysogenization that allow the infected cell to survive. By contrast, population-based protection such as abortive infection systems lead to the cell’s death before phage progeny is released. Here we describe a new role for phage-inducible chromosomal islands (PICIs) in protecting bacterial populations from phage predation. The resulting increased survival has consequences for the acquisition of foreign DNA such as antimicrobial resistance and fitness genes by the prey population as it also allows for the increased survival of bacteria that have acquired new genetic material. As a direct consequence of this increased survival, PICIs expand genetic diversity in bacterial populations. Such increased genetic diversity is advantageous to the complete bacterial population as the best adapted clones will outcompete others in any given environment. PICIs therefore also act as key mediators of population diversification.
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