Shenzhen Institute of Respiratory Diseases, Second Clinical Medical College (Shenzhen People's Hospital), Jinan University, Guangzhou, China.
The First Affiliated Hospital (Shenzhen People's Hospital), Southern University of Science and Technology, Shenzhen, China.
Microbiol Spectr. 2021 Dec 22;9(3):e0114121. doi: 10.1128/Spectrum.01141-21. Epub 2021 Dec 1.
The emergence of high-level tigecycline resistance mediated by plasmid-borne (X) genes greatly threatens the clinical effectiveness of tigecycline. However, the dissemination pattern of plasmid-borne (X) genes remains unclear. We here recovered (X)-positive Acinetobacter isolates from 684 fecal and environmental samples collected at six livestock farms. Fifteen (X)-positive Acinetobacter isolates were identified, mainly including 9 (X3)- and 5 (X6)-positive Acinetobacter towneri isolates. A clonal dissemination of (X3)-positive A. towneri was detected in a swine farm, while the (X6)-positive A. towneri isolates mainly disseminated sporadically in the same farm. A (X3)-carrying plasmid (pAT181) was self-transmissible from a tigecycline-susceptible A. towneri strain to Acinetobacter baumannii strain ATCC 17978, causing 64- to 512-fold increases in the MIC values of tetracyclines (including tigecycline). Worrisomely, pAT181 was stably maintained and increased the growth rate of strain ATCC 17978. Further identification of (X) genes in 10,680 Acinetobacter genomes retrieved from GenBank revealed that (X3) (= 249), (X5)-like (= 61), and (X6) = 53) were the prevalent alleles mainly carried by four species, and most of them were livestock associated. Phylogenetic analysis showed that most of the (X3)- and (X6)-positive isolates disseminated sporadically. The structures of the (X3), and (X6) plasmidomes were highly diverse, and no epidemic plasmids were detected. However, cross-species and cross-region transmissions of (X3) might have been mediated by several plasmids in a small proportion of strains. Our study implies that horizontal plasmid transfer may be insignificant for the current dissemination of (X3) and (X6) in Acinetobacter strains. Continuous surveillance for (X) genes in the context of One Health is necessary to prevent them from transmitting to humans. Recently identified plasmid-borne (X) genes have greatly challenged the efficiency of tigecycline, a last-resort antibiotic for severe infection, while the dissemination pattern of the plasmid-borne (X) genes remains unclear. In this study, we identified a clonal dissemination of (X3)-positive A. towneri isolates on a swine farm, while the (X6)-positive A. towneri strains mainly disseminated sporadically on the same farm. Of more concern, a (X3)-carrying plasmid was found to be self-transmissible, resulting in enhanced tigecycline resistance and growth rate of the recipient. Further exploration of a global data set of (X)-positive Acinetobacter genomes retrieved from GenBank revealed that most of the (X3)- and (X6)-positive isolates shared a highly distant relationship, and the structures of (X3) and (X6) plasmidomes exhibited high mosaicism. Notably, some of the isolates belong to Acinetobacter species that are opportunistic pathogens and have been identified as sources of nosocomial infections, raising concerns about transmission to humans in the future. Our study evidenced the sporadic dissemination of (X3) and (X6) in Acinetobacter strains and the necessity of continuous surveillance for (X) genes in the context of One Health.
高水平的替加环素耐药性由质粒携带（X）基因介导，这极大地威胁了替加环素的临床疗效。然而，质粒携带（X）基因的传播模式仍不清楚。我们从六个养殖场的 684 份粪便和环境样本中回收了（X）阳性不动杆菌分离株。鉴定出 15 株（X）阳性不动杆菌，主要包括 9 株（X3）和 5 株（X6）阳性的阿氏不动杆菌。在一个猪场中检测到（X3）阳性阿氏不动杆菌的克隆传播，而（X6）阳性阿氏不动杆菌分离株主要在同一猪场中散在传播。一个（X3）携带的质粒（pAT181）可以从一株对替加环素敏感的阿氏不动杆菌菌株自我传递到鲍曼不动杆菌菌株 ATCC 17978，导致四环素（包括替加环素）的 MIC 值增加 64-512 倍。令人担忧的是，pAT181 可以稳定地保持并增加菌株 ATCC 17978 的生长速度。进一步鉴定从 GenBank 中检索到的 10680 株不动杆菌基因组中的（X）基因表明，（X3）（=249）、（X5）样（=61）和（X6）（=53）是主要由四个种属携带的流行等位基因，其中大多数与牲畜有关。系统发育分析表明，大多数（X3）和（X6）阳性分离株呈散在传播。（X3）和（X6）质粒组的结构高度多样化，未检测到流行质粒。然而，（X3）的种间和跨地区传播可能是由少数菌株中的几种质粒介导的。我们的研究表明，水平质粒转移对目前不动杆菌菌株中（X3）和（X6）的传播可能并不重要。在“同一健康”背景下，有必要对（X）基因进行持续监测，以防止它们传播给人类。最近发现的质粒携带（X）基因极大地挑战了替加环素的疗效，替加环素是治疗严重感染的最后一道防线，而质粒携带（X）基因的传播模式仍不清楚。在这项研究中，我们在一个猪场中鉴定到（X3）阳性阿氏不动杆菌分离株的克隆传播，而（X6）阳性阿氏不动杆菌分离株主要在同一猪场中散在传播。更令人担忧的是，发现一个（X3）携带的质粒可以自我传递，导致替加环素耐药性增强和受体生长速度加快。进一步探索从 GenBank 中检索到的全球（X）阳性不动杆菌基因组数据集表明，大多数（X3）和（X6）阳性分离株之间的亲缘关系非常远，（X3）和（X6）质粒组的结构表现出高度的镶嵌性。值得注意的是，一些分离株属于机会致病菌不动杆菌种属，已被确定为医院感染的来源，这令人担忧它们将来会传播给人类。我们的研究证明了（X3）和（X6）在不动杆菌菌株中的散在传播，以及在“同一健康”背景下对（X）基因进行持续监测的必要性。
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