Univ. Bordeaux, INRAE, UMR BFP, F-33882, Villenave d'Ornon, France.
Department of Biological Sciences, Auburn University, Auburn, Alabama, 36849-5414, USA.
Microb Genom. 2024 Nov;10(11). doi: 10.1099/mgen.0.001320.
Clustered regularly interspaced short palindromic repeat (CRISPR)-Cas systems are bacterial defences that target bacteriophages and mobile genetic elements. How these defences evolve in novel host environments remains largely unknown. We studied the evolution of the CRISPR-Cas system in (also named ), a bacterial pathogen of poultry that jumped into a passerine host ~30 years ago. Over the decade following the host shift, all isolates displaying a functional CRISPR-Cas system were found not only to harbour completely new sets of spacers, but the DNA protospacer adjacent motif recognized by the main effector Cas9 (MgCas9) was also different. These changes in CRISPR-Cas diversity and specificity are consistent with a change in the community of phages and mobile elements infecting as it colonized the novel host. In the years following the host shift, we also detected a gradual rise in isolates displaying non-functional MgCas9. After 12 years, all circulating isolates harboured inactive forms only. This loss of CRISPR-Cas function comes at a time when the passerine host is known to have evolved widespread resistance, which in turn drove the evolution of increasing virulence through antagonistic coevolution. Such striking concordance in the rise of inactivated forms of CRISPR-Cas and the evolution of host resistance suggests that the inactivation of the CRISPR-Cas system was necessary for enabling adaptive bacterial responses to host-driven selection. We highlight the need to consider both host and pathogen selection pressures on bacteria for understanding the evolution of CRISPR-Cas systems and the key factors driving the emergence of a pathogenic bacterium in a novel host.
成簇规律间隔短回文重复 (CRISPR)-Cas 系统是细菌防御系统，可靶向噬菌体和移动遗传元件。这些防御系统在新宿主环境中的进化方式在很大程度上仍然未知。我们研究了 CRISPR-Cas 系统在 （也称为 ）中的进化，它是一种禽类病原体，约 30 年前跳跃到雀形目宿主中。在宿主转移后的十年中，所有显示功能性 CRISPR-Cas 系统的分离株不仅被发现拥有全新的间隔区，而且主要效应因子 Cas9（MgCas9）识别的 DNA 原间隔邻近基序也不同。CRISPR-Cas 多样性和特异性的这些变化与噬菌体和移动元件群落的变化一致，这些噬菌体和移动元件感染 ，因为它在新宿主中定殖。在宿主转移后的几年中，我们还检测到非功能性 MgCas9 显示率逐渐升高的情况。12 年后，所有循环分离株仅显示失活形式。CRISPR-Cas 功能的丧失发生在雀形目宿主已经进化出广泛抗性的时候，而这反过来又通过拮抗协同进化推动了毒力的增加。CRISPR-Cas 失活形式的上升和宿主抗性的进化之间惊人的一致性表明，CRISPR-Cas 系统的失活对于使细菌对宿主驱动的选择产生适应性反应是必要的。我们强调需要考虑宿主和病原体对细菌的选择压力，以了解 CRISPR-Cas 系统的进化以及在新宿主中出现致病性细菌的关键因素。
