Jia Ruizhao, Su Wenya, Wang Wenjia, Shi Lulu, Zheng Xinrou, Zhang Youming, Xu Hai, Geng Xueyun, Li Ling, Wang Mingyu, Li Xiang
Changsha Hospital for Maternal & Child Health Care Affiliated to Hunan Normal University, Changsha 410007, China.
State Key Laboratory of Microbial Technology, Microbial Technology Institute, Shandong University, Qingdao 266237, China.
Biology (Basel). 2025 Aug 5;14(8):1000. doi: 10.3390/biology14081000.
The perianal skin is a unique "skin-gut" boundary that serves as a critical hotspot for the exchange and evolution of antibiotic resistance genes (ARGs). However, its role in the dissemination of antimicrobial resistance (AMR) has often been underestimated. To characterize the resistance patterns in the perianal skin environment of patients with perianal diseases and to investigate the drivers of AMR in this niche, a total of 51 bacterial isolates were selected from a historical strain bank containing isolates originally collected from patients with perianal diseases. All the isolates originated from the skin site and were subjected to antimicrobial susceptibility testing, whole-genome sequencing, and co-occurrence network analysis. The analysis revealed a highly structured resistance pattern, dominated by two distinct modules: one representing a classic Staphylococcal resistance platform centered around and the operon, and a broad-spectrum multidrug resistance module in Gram-negative bacteria centered around and predominantly carried by IncFIB and other IncF family plasmids. Further analysis pinpointed IncFIB-type plasmids as potent vehicles driving the efficient dissemination of the latter resistance module. Moreover, numerous unexplained resistance phenotypes were observed in a subset of isolates, indicating the potential presence of emerging and uncharacterized AMR threats. These findings establish the perianal skin as a complex reservoir of multidrug resistance genes and a hub for mobile genetic element exchange, highlighting the necessity of enhanced surveillance and targeted interventions in this clinically important ecological niche.
肛周皮肤是一个独特的“皮肤-肠道”边界，是抗生素耐药基因（ARGs）交换和演变的关键热点。然而，其在抗菌药物耐药性（AMR）传播中的作用常常被低估。为了表征肛周疾病患者肛周皮肤环境中的耐药模式，并调查这一生态位中AMR的驱动因素，从一个历史菌株库中选取了51株细菌分离株，该菌株库包含最初从肛周疾病患者中收集的分离株。所有分离株均来源于皮肤部位，并进行了抗菌药物敏感性测试、全基因组测序和共现网络分析。分析揭示了一种高度结构化的耐药模式，由两个不同的模块主导：一个代表以 和 操纵子为中心的经典葡萄球菌耐药平台，另一个是革兰氏阴性菌中的广谱多药耐药模块，以 为中心，主要由IncFIB和其他IncF家族质粒携带。进一步分析确定IncFIB型质粒是驱动后一个耐药模块高效传播的有效载体。此外，在一部分分离株中观察到许多无法解释的耐药表型，表明可能存在新出现的、未表征的AMR威胁。这些发现将肛周皮肤确立为多药耐药基因的复杂储存库和移动遗传元件交换的中心，突出了加强对这一临床重要生态位的监测和针对性干预的必要性。
