Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria
The emergence of plasmid-mediated tigecycline resistance gene tet(X4) poses a challenging threat to public health. Based on the analysis of tet(X4)-positive plasmids in the NCBI database, we found that the IncX1-type plasmid is one of the most common vectors for spreading tet(X4) gene, but the mecha...
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Frontiers Media S.A.
2021
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oai:doaj.org-article:f5d9c7fbe4d84bdc8c7a76b5d0983d6b2021-11-11T10:18:15ZHistone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria1664-302X10.3389/fmicb.2021.763288https://doaj.org/article/f5d9c7fbe4d84bdc8c7a76b5d0983d6b2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.763288/fullhttps://doaj.org/toc/1664-302XThe emergence of plasmid-mediated tigecycline resistance gene tet(X4) poses a challenging threat to public health. Based on the analysis of tet(X4)-positive plasmids in the NCBI database, we found that the IncX1-type plasmid is one of the most common vectors for spreading tet(X4) gene, but the mechanisms by which these plasmids adapt to host bacteria and maintain the persistence of antibiotic resistance genes (ARGs) remain unclear. Herein, we investigated the underlying mechanisms of how host bacteria modulate the fitness cost of IncX1 plasmids carrying tet(X4) gene. Interestingly, we found that the tet(X4)-bearing IncX1 plasmids encoding H-NS protein imposed low or no fitness cost in Escherichia coli and Klebsiella pneumoniae; instead, they partially promoted the virulence and biofilm formation in host bacteria. Regression analysis revealed that the expression of hns gene in plasmids was positively linked to the relative fitness of host bacteria. Furthermore, when pCE2::hns was introduced, the fitness of tet(X4)-positive IncX1 plasmid pRF55-1 without hns gene was significantly improved, indicating that hns mediates the improvement of fitness. Finally, we showed that the expression of hns gene is negatively correlated with the expression of tet(X4) gene, suggesting that the regulatory effect of H-NS on adaptability may be attributed to its inhibitory effect on the expression of ARGs. Together, our findings suggest the important role of plasmid-encoded H-NS protein in modulating the fitness of tet(X4)-bearing IncX1 plasmids, which shed new insight into the dissemination of tet(X4) gene in a biological environment.Wenhui CaiFeifei TangLijie JiangRuichao LiRuichao LiRuichao LiRuichao LiZhiqiang WangZhiqiang WangZhiqiang WangYuan LiuYuan LiuYuan LiuYuan LiuFrontiers Media S.A.articleH-NS proteinfitnesstet(X4)IncX1 plasmidsGram-negative bacteria (GNB)MicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021) |
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H-NS protein fitness tet(X4) IncX1 plasmids Gram-negative bacteria (GNB) Microbiology QR1-502 |
| spellingShingle |
H-NS protein fitness tet(X4) IncX1 plasmids Gram-negative bacteria (GNB) Microbiology QR1-502 Wenhui Cai Feifei Tang Lijie Jiang Ruichao Li Ruichao Li Ruichao Li Ruichao Li Zhiqiang Wang Zhiqiang Wang Zhiqiang Wang Yuan Liu Yuan Liu Yuan Liu Yuan Liu Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria |
| description |
The emergence of plasmid-mediated tigecycline resistance gene tet(X4) poses a challenging threat to public health. Based on the analysis of tet(X4)-positive plasmids in the NCBI database, we found that the IncX1-type plasmid is one of the most common vectors for spreading tet(X4) gene, but the mechanisms by which these plasmids adapt to host bacteria and maintain the persistence of antibiotic resistance genes (ARGs) remain unclear. Herein, we investigated the underlying mechanisms of how host bacteria modulate the fitness cost of IncX1 plasmids carrying tet(X4) gene. Interestingly, we found that the tet(X4)-bearing IncX1 plasmids encoding H-NS protein imposed low or no fitness cost in Escherichia coli and Klebsiella pneumoniae; instead, they partially promoted the virulence and biofilm formation in host bacteria. Regression analysis revealed that the expression of hns gene in plasmids was positively linked to the relative fitness of host bacteria. Furthermore, when pCE2::hns was introduced, the fitness of tet(X4)-positive IncX1 plasmid pRF55-1 without hns gene was significantly improved, indicating that hns mediates the improvement of fitness. Finally, we showed that the expression of hns gene is negatively correlated with the expression of tet(X4) gene, suggesting that the regulatory effect of H-NS on adaptability may be attributed to its inhibitory effect on the expression of ARGs. Together, our findings suggest the important role of plasmid-encoded H-NS protein in modulating the fitness of tet(X4)-bearing IncX1 plasmids, which shed new insight into the dissemination of tet(X4) gene in a biological environment. |
| format |
article |
| author |
Wenhui Cai Feifei Tang Lijie Jiang Ruichao Li Ruichao Li Ruichao Li Ruichao Li Zhiqiang Wang Zhiqiang Wang Zhiqiang Wang Yuan Liu Yuan Liu Yuan Liu Yuan Liu |
| author_facet |
Wenhui Cai Feifei Tang Lijie Jiang Ruichao Li Ruichao Li Ruichao Li Ruichao Li Zhiqiang Wang Zhiqiang Wang Zhiqiang Wang Yuan Liu Yuan Liu Yuan Liu Yuan Liu |
| author_sort |
Wenhui Cai |
| title |
Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria |
| title_short |
Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria |
| title_full |
Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria |
| title_fullStr |
Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria |
| title_full_unstemmed |
Histone-Like Nucleoid Structuring Protein Modulates the Fitness of tet(X4)-Bearing IncX1 Plasmids in Gram-Negative Bacteria |
| title_sort |
histone-like nucleoid structuring protein modulates the fitness of tet(x4)-bearing incx1 plasmids in gram-negative bacteria |
| publisher |
Frontiers Media S.A. |
| publishDate |
2021 |
| url |
https://doaj.org/article/f5d9c7fbe4d84bdc8c7a76b5d0983d6b |
| work_keys_str_mv |
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| _version_ |
1718439274711351296 |