The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii

Although various mechanisms of carbapenem-resistance have been identified in the nosocomial pathogen Acinetobacter baumannii, the critical process of resistance evolution and the factors involved in are not well understood. Herein, we identified a universal stress protein Usp1413 which played an imp...

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Main Authors: Sirui Zhang, Jingdan Wang, Rong Yu, Haiping Liu, Shuyan Liu, Kai Luo, Jin'e Lei, Bei Han, Yanjiong Chen, Shaoshan Han, E Yang, Meng Xun, Lei Han
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Current Research in Microbial Sciences
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666517424001159
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author Sirui Zhang
Jingdan Wang
Rong Yu
Haiping Liu
Shuyan Liu
Kai Luo
Jin'e Lei
Bei Han
Yanjiong Chen
Shaoshan Han
E Yang
Meng Xun
Lei Han
author_facet Sirui Zhang
Jingdan Wang
Rong Yu
Haiping Liu
Shuyan Liu
Kai Luo
Jin'e Lei
Bei Han
Yanjiong Chen
Shaoshan Han
E Yang
Meng Xun
Lei Han
author_sort Sirui Zhang
collection DOAJ
description Although various mechanisms of carbapenem-resistance have been identified in the nosocomial pathogen Acinetobacter baumannii, the critical process of resistance evolution and the factors involved in are not well understood. Herein, we identified a universal stress protein Usp1413 which played an important role in adaptive resistance of A. baumannii to meropenem (MEM). Based on RNA-Seq and genome sequencing, Usp1413 was not only one of the most downregulated USPs, but also the bare one having mutation of tyrosine and glycine inserted at the site of 229-230 (YG229-230) under the stimulation of MEM. Deletion of Usp1413 resulted in increased MEM resistance. In addition, Usp1413 affected the bacterial abilities of biofilm formation and swarm motility, as well as helped A. baumannii response to various environmental stresses. These effects of Usp1413 were achieved by regulating its interaction proteins, within the functions of YigZ family protein, acetyltransferase, and SulP family inorganic anion transporter. The insertion mutation of YG229-230 influenced both the expression of interaction proteins and the phenotypes of bacteria. Finally, the promotor region of Usp1413 was convinced by point mutations. Overall, our findings identified the universal stress protein Usp1413 as a contributor involved in MEM adaptive resistance and responded to numerous environmental stresses. This study provides novel insights into the mechanism of universal stress proteins in participating antibiotic resistance, and affords a potential target for controlling drug resistance development in A. baumannii.
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spelling doaj-art-0da318bbbabe4811bac1a9ff446396752025-08-20T02:35:44ZengElsevierCurrent Research in Microbial Sciences2666-51742025-01-01810033210.1016/j.crmicr.2024.100332The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumanniiSirui Zhang0Jingdan Wang1Rong Yu2Haiping Liu3Shuyan Liu4Kai Luo5Jin'e Lei6Bei Han7Yanjiong Chen8Shaoshan Han9E Yang10Meng Xun11Lei Han12Department of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaSchool of Public Health, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaSchool of Public Health, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, China; Xi'an Daxing Hospital, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Laboratory Medicine, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, ChinaSchool of Public Health, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Hepatobiliary Surgery, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, ChinaDepartment of Microbiology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University Health Science Center, Xi'an, China; Corresponding author.Although various mechanisms of carbapenem-resistance have been identified in the nosocomial pathogen Acinetobacter baumannii, the critical process of resistance evolution and the factors involved in are not well understood. Herein, we identified a universal stress protein Usp1413 which played an important role in adaptive resistance of A. baumannii to meropenem (MEM). Based on RNA-Seq and genome sequencing, Usp1413 was not only one of the most downregulated USPs, but also the bare one having mutation of tyrosine and glycine inserted at the site of 229-230 (YG229-230) under the stimulation of MEM. Deletion of Usp1413 resulted in increased MEM resistance. In addition, Usp1413 affected the bacterial abilities of biofilm formation and swarm motility, as well as helped A. baumannii response to various environmental stresses. These effects of Usp1413 were achieved by regulating its interaction proteins, within the functions of YigZ family protein, acetyltransferase, and SulP family inorganic anion transporter. The insertion mutation of YG229-230 influenced both the expression of interaction proteins and the phenotypes of bacteria. Finally, the promotor region of Usp1413 was convinced by point mutations. Overall, our findings identified the universal stress protein Usp1413 as a contributor involved in MEM adaptive resistance and responded to numerous environmental stresses. This study provides novel insights into the mechanism of universal stress proteins in participating antibiotic resistance, and affords a potential target for controlling drug resistance development in A. baumannii.http://www.sciencedirect.com/science/article/pii/S2666517424001159Acinetobacter baumanniiUniversal stress protein Usp1413Adaptive resistance to meropenemBiofilm formationSwarming motilityEnvironmental stresses
spellingShingle Sirui Zhang
Jingdan Wang
Rong Yu
Haiping Liu
Shuyan Liu
Kai Luo
Jin'e Lei
Bei Han
Yanjiong Chen
Shaoshan Han
E Yang
Meng Xun
Lei Han
The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii
Current Research in Microbial Sciences
Acinetobacter baumannii
Universal stress protein Usp1413
Adaptive resistance to meropenem
Biofilm formation
Swarming motility
Environmental stresses
title The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii
title_full The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii
title_fullStr The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii
title_full_unstemmed The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii
title_short The role of universal stress protein Usp1413 in meropenem adaptive resistance and environmental stress responses in Acinetobacter baumannii
title_sort role of universal stress protein usp1413 in meropenem adaptive resistance and environmental stress responses in acinetobacter baumannii
topic Acinetobacter baumannii
Universal stress protein Usp1413
Adaptive resistance to meropenem
Biofilm formation
Swarming motility
Environmental stresses
url http://www.sciencedirect.com/science/article/pii/S2666517424001159
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