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

Author

Listed:
  • Xia Li

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

  • Wenfang Yin

    (South China Agricultural University)

  • Junjie Desmond Lin

    (Nanyang Technological University)

  • Yong Zhang

    (Southwest University)

  • Quan Guo

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

  • Gerun Wang

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

  • Xiayu Chen

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

  • Binbin Cui

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

  • Mingfang Wang

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

  • Min Chen

    (Southwest University)

  • Peng Li

    (Hainan Normal University)

  • Ya-Wen He

    (Shanghai Jiao Tong University)

  • Wei Qian

    (Chinese Academy of Sciences)

  • Haibin Luo

    (Hainan University)

  • Lian-Hui Zhang

    (South China Agricultural University)

  • Xue-Wei Liu

    (Nanyang Technological University)

  • Shihao Song

    (Hainan University)

  • Yinyue Deng

    (Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University)

Abstract

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.

Suggested Citation

  • Xia Li & Wenfang Yin & Junjie Desmond Lin & Yong Zhang & Quan Guo & Gerun Wang & Xiayu Chen & Binbin Cui & Mingfang Wang & Min Chen & Peng Li & Ya-Wen He & Wei Qian & Haibin Luo & Lian-Hui Zhang & Xue, 2023. "Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2′,3′-cyclic guanosine monophosphate," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43461-2
    DOI: 10.1038/s41467-023-43461-2
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    1. Aaron T. Whiteley & James B. Eaglesham & Carina C. de Oliveira Mann & Benjamin R. Morehouse & Brianna Lowey & Eric A. Nieminen & Olga Danilchanka & David S. King & Amy S. Y. Lee & John J. Mekalanos & , 2019. "Bacterial cGAS-like enzymes synthesize diverse nucleotide signals," Nature, Nature, vol. 567(7747), pages 194-199, March.
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    3. Kyle A. Floyd & Calvin K. Lee & Wujing Xian & Mahmoud Nametalla & Aneesa Valentine & Benjamin Crair & Shiwei Zhu & Hannah Q. Hughes & Jennifer L. Chlebek & Daniel C. Wu & Jin Hwan Park & Ali M. Farhat, 2020. "c-di-GMP modulates type IV MSHA pilus retraction and surface attachment in Vibrio cholerae," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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