Gu Weihan, Chen Yufan, Xie Congcong, Chen Zhongqiao, Gao Huagui, Zhu Yaping, Zhang Lian-Hui, Liao Lisheng
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, China.
Research 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, China.
mBio. 2025 Jul 9;16(7):e0101625. doi: 10.1128/mbio.01016-25. Epub 2025 May 30.
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 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.IMPORTANCE 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 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 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.
是一种能够感染多种农作物和植物的常见病原体，其细胞运动性在侵染宿主及随后的系统感染中起关键作用。我们最近证明，细菌第二信使环二鸟苷酸（c-di-GMP）和腐胺（PUT）介导的群体感应（QS）系统分别参与细菌运动性的负调控和正调控，反之亦然，它们还参与生物膜形成的调控。在本研究中，我们旨在探究这两种信号传导机制在调节细菌运动性方面的潜在相互作用。结果表明，PUT系统的无效突变似乎对c-di-GMP的细胞水平影响不大；然而，编码c-di-GMP降解的基因缺失导致PUT产生显著减少。随后的一项研究揭示，第二信使信号系统通过c-di-GMP受体YcgR与腐胺QS系统相互作用。这种相互作用增强了SpeA的活性，SpeA是腐胺生物合成途径中的限速酶，导致细胞内腐胺水平升高。至关重要的是，这种促进作用被c-di-GMP分子抑制；因此，SpeA、YcgR和c-di-GMP构成了一个通过控制腐胺生物合成速率来调节运动性的调控环。本研究结果首次揭示了细菌中c-di-GMP与腐胺信号系统之间的相互作用机制。重要性是一种重要的细菌病原体，可感染多种植物和作物，导致重大经济损失，尤其是在水稻和香蕉种植中。细菌运动性是其关键致病因素，因为它使病原体能够竞争食物资源并侵染宿主植物。这种运动性受到第二信使c-di-GMP的负调控和群体感应信号腐胺（PUT）的正调控。然而，c-di-GMP和PUT信号系统在调节运动性方面的潜在联系尚未明确。在此，我们揭示了它们之间相互作用的联系和机制，证明c-di-GMP通过其受体YcgR与PUT系统相互作用。我们研究的意义在于首次揭示了c-di-GMP和PUT信号网络之间的分子相互作用，这两种信号机制广泛保守，并阐明了控制细菌运动性和毒力的复杂精细调控机制。
