The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility
ABSTRACT Dickeya oryzae is a prevalent pathogen capable of infecting a variety of crops and plants, and its cell motility plays a key role in invasion of host and subsequent systemic infection. We recently demonstrated that the bacterial second messenger c-di-GMP and the putrescine (PUT)-mediated qu...
Saved in:
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2025-07-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.01016-25 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849428491897929728 |
|---|---|
| author | Weihan Gu Yufan Chen Congcong Xie Zhongqiao Chen Huagui Gao Yaping Zhu Lian-hui Zhang Lisheng Liao |
| author_facet | Weihan Gu Yufan Chen Congcong Xie Zhongqiao Chen Huagui Gao Yaping Zhu Lian-hui Zhang Lisheng Liao |
| author_sort | Weihan Gu |
| collection | DOAJ |
| description | ABSTRACT Dickeya oryzae is a prevalent pathogen capable of infecting a variety of crops and plants, and its cell motility plays a key role in invasion of host and subsequent systemic infection. We recently demonstrated that the bacterial second messenger c-di-GMP and the putrescine (PUT)-mediated quorum sensing (QS) system are, respectively, involved in negative and positive regulation of bacterial motility, and vice versa, biofilm formation. In this study, we aimed to investigate the potential interaction of these two signaling mechanisms in the modulation of bacterial motility. The results indicated that null mutation of the PUT system did not seem to have much effect on the cellular level of c-di-GMP; however, deletion of the genes encoding c-di-GMP degradation led to a significant reduction in PUT production. A subsequent study unveiled that the second messenger signaling system interacted with the putrescine QS system through the c-di-GMP receptor YcgR. This interaction enhanced the activity of SpeA, which is the rate-limiting enzyme in the putrescine biosynthesis pathway, resulting in increased intracellular putrescine level. Critically, this facilitative effect was inhibited by c-di-GMP molecules; thus, SpeA, YcgR, and c-di-GMP constitute a regulatory loop modulating D. oryzae motility by controlling the rate of putrescine biosynthesis. The findings from this study provide the first insight into the interaction mechanism between c-di-GMP and putrescine signaling systems in bacteria.IMPORTANCEDickeya oryzae is an important bacterial pathogen that can infect numerous plants and crops, leading to substantial economic losses, especially in rice and banana cultivation. Bacterial motility is a crucial pathogenic factor for D. oryzae as it enables the pathogen to compete for food resources and invade host plants. This motility is negatively regulated by the second messenger c-di-GMP and positively regulated by the quorum sensing signal putrescine (PUT). However, the potential connection between c-di-GMP and PUT signaling systems in regulating the motility of D. oryzae has not been understood. Here, we reveal the link and mechanism of the interaction between them, demonstrating that c-di-GMP interacts with the PUT system via its receptor YcgR. The significance of our research lies in providing the first insight into the molecular interaction between c-di-GMP and PUT signaling networks, both of which are widely conserved signaling mechanisms, and sheds light on the complex and sophisticated regulatory mechanisms that govern bacterial motility and virulence. |
| format | Article |
| id | doaj-art-6557780035d842529ffabd9351373946 |
| institution | Kabale University |
| issn | 2150-7511 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj-art-6557780035d842529ffabd93513739462025-08-20T03:28:41ZengAmerican Society for MicrobiologymBio2150-75112025-07-0116710.1128/mbio.01016-25The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motilityWeihan Gu0Yufan Chen1Congcong Xie2Zhongqiao Chen3Huagui Gao4Yaping Zhu5Lian-hui Zhang6Lisheng Liao7Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaResearch Center of Chinese Herbal Resource Science and Engineering, Key Laboratory of Chinese Medicinal Resource From Lingnan, Ministry of Education, Joint Laboratory of National Engineering Research Center for the Pharmaceutics of Traditional Chinese Medicines, Guangzhou University of Chinese Medicine, Guangzhou, ChinaSchool of Biological and Environmental Engineering, Jingdezhen University, Jingdezhen, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaABSTRACT Dickeya oryzae is a prevalent pathogen capable of infecting a variety of crops and plants, and its cell motility plays a key role in invasion of host and subsequent systemic infection. We recently demonstrated that the bacterial second messenger c-di-GMP and the putrescine (PUT)-mediated quorum sensing (QS) system are, respectively, involved in negative and positive regulation of bacterial motility, and vice versa, biofilm formation. In this study, we aimed to investigate the potential interaction of these two signaling mechanisms in the modulation of bacterial motility. The results indicated that null mutation of the PUT system did not seem to have much effect on the cellular level of c-di-GMP; however, deletion of the genes encoding c-di-GMP degradation led to a significant reduction in PUT production. A subsequent study unveiled that the second messenger signaling system interacted with the putrescine QS system through the c-di-GMP receptor YcgR. This interaction enhanced the activity of SpeA, which is the rate-limiting enzyme in the putrescine biosynthesis pathway, resulting in increased intracellular putrescine level. Critically, this facilitative effect was inhibited by c-di-GMP molecules; thus, SpeA, YcgR, and c-di-GMP constitute a regulatory loop modulating D. oryzae motility by controlling the rate of putrescine biosynthesis. The findings from this study provide the first insight into the interaction mechanism between c-di-GMP and putrescine signaling systems in bacteria.IMPORTANCEDickeya oryzae is an important bacterial pathogen that can infect numerous plants and crops, leading to substantial economic losses, especially in rice and banana cultivation. Bacterial motility is a crucial pathogenic factor for D. oryzae as it enables the pathogen to compete for food resources and invade host plants. This motility is negatively regulated by the second messenger c-di-GMP and positively regulated by the quorum sensing signal putrescine (PUT). However, the potential connection between c-di-GMP and PUT signaling systems in regulating the motility of D. oryzae has not been understood. Here, we reveal the link and mechanism of the interaction between them, demonstrating that c-di-GMP interacts with the PUT system via its receptor YcgR. The significance of our research lies in providing the first insight into the molecular interaction between c-di-GMP and PUT signaling networks, both of which are widely conserved signaling mechanisms, and sheds light on the complex and sophisticated regulatory mechanisms that govern bacterial motility and virulence.https://journals.asm.org/doi/10.1128/mbio.01016-25Dickeya oryzaec-di-GMPputrescinebacterial motilityYcgR |
| spellingShingle | Weihan Gu Yufan Chen Congcong Xie Zhongqiao Chen Huagui Gao Yaping Zhu Lian-hui Zhang Lisheng Liao The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility mBio Dickeya oryzae c-di-GMP putrescine bacterial motility YcgR |
| title | The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility |
| title_full | The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility |
| title_fullStr | The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility |
| title_full_unstemmed | The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility |
| title_short | The cyclic di-GMP receptor YcgR links the second messenger with the putrescine quorum sensing system in modulation of Dickeya oryzae motility |
| title_sort | cyclic di gmp receptor ycgr links the second messenger with the putrescine quorum sensing system in modulation of dickeya oryzae motility |
| topic | Dickeya oryzae c-di-GMP putrescine bacterial motility YcgR |
| url | https://journals.asm.org/doi/10.1128/mbio.01016-25 |
| work_keys_str_mv | AT weihangu thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT yufanchen thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT congcongxie thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT zhongqiaochen thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT huaguigao thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT yapingzhu thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT lianhuizhang thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT lishengliao thecyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT weihangu cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT yufanchen cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT congcongxie cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT zhongqiaochen cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT huaguigao cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT yapingzhu cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT lianhuizhang cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility AT lishengliao cyclicdigmpreceptorycgrlinksthesecondmessengerwiththeputrescinequorumsensingsysteminmodulationofdickeyaoryzaemotility |