Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation
Carbapenem-resistant Enterobacteriaceae (CRE) are a critical public health problem worldwide. Globally, IncX3-type plasmids have emerged as the predominant vehicles carrying the metallo-β-lactamase gene blaNDM. Although blaNDM-bearing IncX3 plasmids have been found in various hosts from diverse envi...
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| Format: | Article |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.765492/full |
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| author | Liu Baomo Liu Baomo Shui Lili Robert A. Moran Willem van Schaik Zhuo Chao |
| author_facet | Liu Baomo Liu Baomo Shui Lili Robert A. Moran Willem van Schaik Zhuo Chao |
| author_sort | Liu Baomo |
| collection | DOAJ |
| description | Carbapenem-resistant Enterobacteriaceae (CRE) are a critical public health problem worldwide. Globally, IncX3-type plasmids have emerged as the predominant vehicles carrying the metallo-β-lactamase gene blaNDM. Although blaNDM-bearing IncX3 plasmids have been found in various hosts from diverse environments, whether their transfer and persistence properties vary under different conditions and what factors influence any variation is unknown. By observing the effects of different temperatures on IncX3 plasmid conjugation rates, stability, and effects on host fitness in Escherichia coli, we demonstrate that temperature is an important determinant of plasmid phenotypes. The IncX3 plasmid pGZIncX3 transferred at highest frequencies, was most stable and imposed lower fitness costs at 37°C. Temperature-regulated variation in pGZIncX3 properties involved a thermoregulated plasmid-encoded H-NS-like protein, which was produced at higher levels at 30°C and 42°C and inhibited the expression of type IV secretion system genes involved in conjugation. These findings suggest that blaNDM-bearing IncX3 plasmids are adapted to carriage by enterobacteria that colonize mammalian hosts and could explain the rapid dissemination of these plasmids among human-associated species, particularly in hospital settings. |
| first_indexed | 2024-12-24T01:33:58Z |
| format | Article |
| id | doaj.art-6b01a6f4fb9548a8a9d2aa4ef56c1c73 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-24T01:33:58Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-6b01a6f4fb9548a8a9d2aa4ef56c1c732022-12-21T17:22:16ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-01-011210.3389/fmicb.2021.765492765492Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in ThermoregulationLiu Baomo0Liu Baomo1Shui Lili2Robert A. Moran3Willem van Schaik4Zhuo Chao5State Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, ChinaDepartment of Respiratory and Critical Care Medicine, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou, ChinaDepartment of Pulmonary and Critical Care Medicine, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaInstitute of Microbiology and Infection, University of Birmingham, Birmingham, United KingdomInstitute of Microbiology and Infection, University of Birmingham, Birmingham, United KingdomState Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, ChinaCarbapenem-resistant Enterobacteriaceae (CRE) are a critical public health problem worldwide. Globally, IncX3-type plasmids have emerged as the predominant vehicles carrying the metallo-β-lactamase gene blaNDM. Although blaNDM-bearing IncX3 plasmids have been found in various hosts from diverse environments, whether their transfer and persistence properties vary under different conditions and what factors influence any variation is unknown. By observing the effects of different temperatures on IncX3 plasmid conjugation rates, stability, and effects on host fitness in Escherichia coli, we demonstrate that temperature is an important determinant of plasmid phenotypes. The IncX3 plasmid pGZIncX3 transferred at highest frequencies, was most stable and imposed lower fitness costs at 37°C. Temperature-regulated variation in pGZIncX3 properties involved a thermoregulated plasmid-encoded H-NS-like protein, which was produced at higher levels at 30°C and 42°C and inhibited the expression of type IV secretion system genes involved in conjugation. These findings suggest that blaNDM-bearing IncX3 plasmids are adapted to carriage by enterobacteria that colonize mammalian hosts and could explain the rapid dissemination of these plasmids among human-associated species, particularly in hospital settings.https://www.frontiersin.org/articles/10.3389/fmicb.2021.765492/fullIncX3carbapenem resistance Enterobacteriaceaetemperatureplasmid-encoded hnsfitness |
| spellingShingle | Liu Baomo Liu Baomo Shui Lili Robert A. Moran Willem van Schaik Zhuo Chao Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation Frontiers in Microbiology IncX3 carbapenem resistance Enterobacteriaceae temperature plasmid-encoded hns fitness |
| title | Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation |
| title_full | Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation |
| title_fullStr | Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation |
| title_full_unstemmed | Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation |
| title_short | Temperature-Regulated IncX3 Plasmid Characteristics and the Role of Plasmid-Encoded H-NS in Thermoregulation |
| title_sort | temperature regulated incx3 plasmid characteristics and the role of plasmid encoded h ns in thermoregulation |
| topic | IncX3 carbapenem resistance Enterobacteriaceae temperature plasmid-encoded hns fitness |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.765492/full |
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