Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate

Previous studies have demonstrated that bis-(3',5')-cyclic diguanosine monophosphate (bis-3',5'-c-di-GMP) is a ubiquitous second messenger employed by bacteria. Here, we report that 2',3'-cyclic guanosine monophosphate (2',3'-cGMP) controls the important biolo...

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Main Authors: Li, Xia, Yin, Wenfang, Lin, Desmond Junjie, Zhang, Yong, Guo, Quan, Wang, Gerun, Chen, Xiayu, Cui, Binbin, Wang, Mingfang, Chen, Min, Li, Peng, He, Ya-Wen, Qian, Wei, Luo, Haibin, Zhang, Lian-Hui, Liu, Xue-Wei, Song, Shihao, Deng, Yinyue
Other Authors: School of Physical and Mathematical Sciences
Format: Article
Language:English
Published: 2024
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Online Access:https://hdl.handle.net/10356/172996
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spelling sg-ntu-dr.10356-1729962024-01-08T15:35:06Z Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate Li, Xia Yin, Wenfang Lin, Desmond Junjie Zhang, Yong Guo, Quan Wang, Gerun Chen, Xiayu Cui, Binbin Wang, Mingfang Chen, Min Li, Peng He, Ya-Wen Qian, Wei Luo, Haibin Zhang, Lian-Hui Liu, Xue-Wei Song, Shihao Deng, Yinyue School of Physical and Mathematical Sciences Science::Chemistry Guanosine Monophosphate Ralstonia Solanacearum Previous studies have demonstrated that bis-(3',5')-cyclic diguanosine monophosphate (bis-3',5'-c-di-GMP) is a ubiquitous second messenger employed by bacteria. Here, we report that 2',3'-cyclic guanosine monophosphate (2',3'-cGMP) controls the important biological functions, quorum sensing (QS) signaling systems and virulence in Ralstonia solanacearum through the transcriptional regulator RSp0980. This signal specifically binds to RSp0980 with high affinity and thus abolishes the interaction between RSp0980 and the promoters of target genes. In-frame deletion of RSp0334, which contains an evolved GGDEF domain with a LLARLGGDQF motif required to catalyze 2',3'-cGMP to (2',5')(3',5')-cyclic diguanosine monophosphate (2',3'-c-di-GMP), altered the abovementioned important phenotypes through increasing the intracellular 2',3'-cGMP levels. Furthermore, we found that 2',3'-cGMP, its receptor and the evolved GGDEF domain with a LLARLGGDEF motif also exist in the human pathogen Salmonella typhimurium. Together, our work provides insights into the unusual function of the GGDEF domain of RSp0334 and the special regulatory mechanism of 2',3'-cGMP signal in bacteria. Published version This work was financially supported by the National Key Research and Development Program of China (2021YFA0717003 to Y.D.) and the Science, Technology and Innovation Commission of Shenzhen Municipality (JCYJ20200109142416497 to Y.D.), the National Natural Science Foundation of China (32300033 to S.S.), and Project Funded by China Postdoctoral Science Foundation (2022M713634 to S.S). 2024-01-08T05:58:34Z 2024-01-08T05:58:34Z 2023 Journal Article Li, X., Yin, W., Lin, D. J., Zhang, Y., Guo, Q., Wang, G., Chen, X., Cui, B., Wang, M., Chen, M., Li, P., He, Y., Qian, W., Luo, H., Zhang, L., Liu, X., Song, S. & Deng, Y. (2023). Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate. Nature Communications, 14(1), 7654-. https://dx.doi.org/10.1038/s41467-023-43461-2 2041-1723 https://hdl.handle.net/10356/172996 10.1038/s41467-023-43461-2 37996405 2-s2.0-85177696511 1 14 7654 en Nature Communications © 2023 The Author(s). Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/ licenses/by/4.0/. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Chemistry
Guanosine Monophosphate
Ralstonia Solanacearum
spellingShingle Science::Chemistry
Guanosine Monophosphate
Ralstonia Solanacearum
Li, Xia
Yin, Wenfang
Lin, Desmond Junjie
Zhang, Yong
Guo, Quan
Wang, Gerun
Chen, Xiayu
Cui, Binbin
Wang, Mingfang
Chen, Min
Li, Peng
He, Ya-Wen
Qian, Wei
Luo, Haibin
Zhang, Lian-Hui
Liu, Xue-Wei
Song, Shihao
Deng, Yinyue
Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
description Previous studies have demonstrated that bis-(3',5')-cyclic diguanosine monophosphate (bis-3',5'-c-di-GMP) is a ubiquitous second messenger employed by bacteria. Here, we report that 2',3'-cyclic guanosine monophosphate (2',3'-cGMP) controls the important biological functions, quorum sensing (QS) signaling systems and virulence in Ralstonia solanacearum through the transcriptional regulator RSp0980. This signal specifically binds to RSp0980 with high affinity and thus abolishes the interaction between RSp0980 and the promoters of target genes. In-frame deletion of RSp0334, which contains an evolved GGDEF domain with a LLARLGGDQF motif required to catalyze 2',3'-cGMP to (2',5')(3',5')-cyclic diguanosine monophosphate (2',3'-c-di-GMP), altered the abovementioned important phenotypes through increasing the intracellular 2',3'-cGMP levels. Furthermore, we found that 2',3'-cGMP, its receptor and the evolved GGDEF domain with a LLARLGGDEF motif also exist in the human pathogen Salmonella typhimurium. Together, our work provides insights into the unusual function of the GGDEF domain of RSp0334 and the special regulatory mechanism of 2',3'-cGMP signal in bacteria.
author2 School of Physical and Mathematical Sciences
author_facet School of Physical and Mathematical Sciences
Li, Xia
Yin, Wenfang
Lin, Desmond Junjie
Zhang, Yong
Guo, Quan
Wang, Gerun
Chen, Xiayu
Cui, Binbin
Wang, Mingfang
Chen, Min
Li, Peng
He, Ya-Wen
Qian, Wei
Luo, Haibin
Zhang, Lian-Hui
Liu, Xue-Wei
Song, Shihao
Deng, Yinyue
format Article
author Li, Xia
Yin, Wenfang
Lin, Desmond Junjie
Zhang, Yong
Guo, Quan
Wang, Gerun
Chen, Xiayu
Cui, Binbin
Wang, Mingfang
Chen, Min
Li, Peng
He, Ya-Wen
Qian, Wei
Luo, Haibin
Zhang, Lian-Hui
Liu, Xue-Wei
Song, Shihao
Deng, Yinyue
author_sort Li, Xia
title Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
title_short Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
title_full Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
title_fullStr Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
title_full_unstemmed Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
title_sort regulation of the physiology and virulence of ralstonia solanacearum by the second messenger 2',3'-cyclic guanosine monophosphate
publishDate 2024
url https://hdl.handle.net/10356/172996
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