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Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence
The zeamines produced by Dickeya oryzae are potent polyamine antibiotics and phytotoxins that are essential for bacterial virulence. We recently showed that the RND efflux pump DesABC in D. oryzae confers partial resistance to zeamines. To fully elucidate the bacterial self‐protection mechanisms, in...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10632790/ https://www.ncbi.nlm.nih.gov/pubmed/37740253 http://dx.doi.org/10.1111/mpp.13386 |
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author | Liang, Zhibin Huang, Luhao Liu, Huidi Zheng, Ying Feng, Jiani Shi, Zurong Chen, Yufan Lv, Mingfa Zhou, Jianuan Zhang, Lian‐Hui Chen, Shaohua |
author_facet | Liang, Zhibin Huang, Luhao Liu, Huidi Zheng, Ying Feng, Jiani Shi, Zurong Chen, Yufan Lv, Mingfa Zhou, Jianuan Zhang, Lian‐Hui Chen, Shaohua |
author_sort | Liang, Zhibin |
collection | PubMed |
description | The zeamines produced by Dickeya oryzae are potent polyamine antibiotics and phytotoxins that are essential for bacterial virulence. We recently showed that the RND efflux pump DesABC in D. oryzae confers partial resistance to zeamines. To fully elucidate the bacterial self‐protection mechanisms, in this study we used transposon mutagenesis to identify the genes encoding proteins involved in zeamine resistance in D. oryzae EC1. This led to the identification of a seven‐gene operon, arn (EC1), that encodes enzyme homologues associated with lipopolysaccharide modification. Deletion of the arn (EC1) genes in strain EC1 compromised its zeamine resistance 8‐ to 16‐fold. Further deletion of the des gene in the arn (EC1) mutant background reduced zeamine resistance to a level similar to that of the zeamine‐sensitive Escherichia coli DH5α. Intriguingly, the arn (EC1) mutants showed varied bacterial virulence on rice, potato, and Chinese cabbage. Further analyses demonstrated that ArnBCAT(EC1) are involved in maintenance of the bacterial nonmucoid morphotype by repressing the expression of capsular polysaccharide genes and that ArnB(EC1) is a bacterial virulence determinant, influencing transcriptional expression of over 650 genes and playing a key role in modulating bacterial motility and virulence. Taken together, these findings decipher a novel zeamine resistance mechanism in D. oryzae and document new roles of the Arn enzymes in modulation of bacterial physiology and virulence. |
format | Online Article Text |
id | pubmed-10632790 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-106327902023-11-15 Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence Liang, Zhibin Huang, Luhao Liu, Huidi Zheng, Ying Feng, Jiani Shi, Zurong Chen, Yufan Lv, Mingfa Zhou, Jianuan Zhang, Lian‐Hui Chen, Shaohua Mol Plant Pathol Original Articles The zeamines produced by Dickeya oryzae are potent polyamine antibiotics and phytotoxins that are essential for bacterial virulence. We recently showed that the RND efflux pump DesABC in D. oryzae confers partial resistance to zeamines. To fully elucidate the bacterial self‐protection mechanisms, in this study we used transposon mutagenesis to identify the genes encoding proteins involved in zeamine resistance in D. oryzae EC1. This led to the identification of a seven‐gene operon, arn (EC1), that encodes enzyme homologues associated with lipopolysaccharide modification. Deletion of the arn (EC1) genes in strain EC1 compromised its zeamine resistance 8‐ to 16‐fold. Further deletion of the des gene in the arn (EC1) mutant background reduced zeamine resistance to a level similar to that of the zeamine‐sensitive Escherichia coli DH5α. Intriguingly, the arn (EC1) mutants showed varied bacterial virulence on rice, potato, and Chinese cabbage. Further analyses demonstrated that ArnBCAT(EC1) are involved in maintenance of the bacterial nonmucoid morphotype by repressing the expression of capsular polysaccharide genes and that ArnB(EC1) is a bacterial virulence determinant, influencing transcriptional expression of over 650 genes and playing a key role in modulating bacterial motility and virulence. Taken together, these findings decipher a novel zeamine resistance mechanism in D. oryzae and document new roles of the Arn enzymes in modulation of bacterial physiology and virulence. John Wiley and Sons Inc. 2023-09-22 /pmc/articles/PMC10632790/ /pubmed/37740253 http://dx.doi.org/10.1111/mpp.13386 Text en © 2023 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Original Articles Liang, Zhibin Huang, Luhao Liu, Huidi Zheng, Ying Feng, Jiani Shi, Zurong Chen, Yufan Lv, Mingfa Zhou, Jianuan Zhang, Lian‐Hui Chen, Shaohua Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence |
title | Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence |
title_full | Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence |
title_fullStr | Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence |
title_full_unstemmed | Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence |
title_short | Characterization of the Arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in Dickeya oryzae physiology and virulence |
title_sort | characterization of the arn lipopolysaccharide modification system essential for zeamine resistance unveils its new roles in dickeya oryzae physiology and virulence |
topic | Original Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10632790/ https://www.ncbi.nlm.nih.gov/pubmed/37740253 http://dx.doi.org/10.1111/mpp.13386 |
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