strains harboring the CRISPR-Cas system are important foodborne pathogens causing serious neonatal infections. However, the specific role of the CRISPR-Cas system in bacterial evolution remains relatively unexplored. In this study, we investigated the impact of CRISPR-Cas in evolution and obtained 137 new whole-genome sequences of by next-generation sequencing technology. Among the strains examined (n=240), 90.6% (193/213) of prevalent species ,, and strains had intact CRISPR-Cas systems. Two rare species, (n=2) and (n=6), lacked and preserved the CRISPR-Cas system at a low frequency (1/6), respectively. These results suggest that the presence of one CRISPR-Cas system in is important for the species to maintain genome homeostasis for survival. The ancestral strain was likely to harbored both subtype I-E and I-F CRISPR-Cas systems, during the long evolutionary process, subtype I-E was retained, while subtype I-F selectively degenerated in species and was even lost in the major pathovars. Moreover, significantly higher CRISPR activity was observed in plant-associated species than in the virulence-related species and Similar spacers of CRISPR arrays were rarely found among species, suggesting intensive change through adaptive acquisition and loss. Differentiated CRISPR activity appears to be the product of environmental selective pressure and might contribute to the bidirectional divergence and speciation of This study reports the evolutionary history of under the selective pressure of the CRISPR-Cas system. One CRISPR-Cas system in is important for maintaining genome homeostasis, whereas two types of systems may be redundant and not conducive for acquiring beneficial DNA for environmental adaption and pathogenicity. Differentiated CRISPR activity has contributed to the bidirectional divergence and genetic diversity of This perspective makes a significant contribution to the literature by providing new insights into CRISPR-Cas systems in general, while further expanding the roles of CRISPR beyond conferring adaptive immunity and demonstrating a link to adaptation and species divergence in a genus. Moreover, our study provides new insights into the balance between genome homeostasis and the uptake of beneficial DNA related to CRISPR-based activity in the evolution of .