Tricarboxylic Acid (TCA) Cycle Enzymes and Intermediates Modulate Intracellular Cyclic di-GMP Levels and the Production of Plant Cell Wall–Degrading Enzymes in Soft Rot Pathogen Dickeya dadantii

Authors: YUAN, XIAOCHEN - Jiangsu Academy Agricultural Sciences; ZENG, QUAN - Agricultural Experiment Station, Connecticut; XU, JINGSHENG - Chinese Academy Of Agricultural Sciences; SEVERIN, GEOFFREY - Michigan State University; ZHOU, XIANG - Zhejiang A & F University; WATERS, CHRISTOPHER - Michigan State University; SUNDIN, GEORGE - Michigan State University; Ibekwe, Abasiofiok - Mark; LIU, FENGQUAN - University Of Wisconsin; YANG, CHING-HONG - University Of Wisconsin

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/8/2019
Publication Date: 12/18/2019
Citation: Yuan, X., Zeng, Q., Xu, J., Severin, G.B., Zhou, X., Waters, C.M., Ibekwe, A.M., Liu, F., Yang, C. 2020. Systematic study of the TCA cycle in virulence regulation links cyclic di-GMP signaling in Dickeya dadantii. Molecular Plant-Microbe Interactions. 33(2):296-307. https://doi.org/10.1094/MPMI-07-19-0203-R.
DOI: https://doi.org/10.1094/MPMI-07-19-0203-R

Interpretive Summary: Dickeya dadantii is a plant pathogen that causes soft-rot, wilt and blight diseases in a wide range of important vegetables and crops. There are many mechanisms used by this bacterium to cause diseases in plants, and one of the mechanisms is the use of the citric acid cycle. In this study, we performed DNA work to advance our knowledge of citric acid enzymes that help Dickeya dadantii cause different kinds of diseases. Our study proposed a novel signaling cascade in controlling the virulence of D. dadantii, by which bacterial metabolism is linked with secondary messengers. The results of this research will be used by growers, researchers, and different state agencies that are involved in cabbage, tomato and chicory production.

Technical Abstract: Dickeya dadantii is a plant pathogenic bacterium that can infect a wide range of plant hosts and organs. Previously, we showed that cyclic di-GMP (c-di-GMP), a bacterial secondary messenger, plays a critical role in the regulation of D. dadantii virulence. Here, we demonstrate an intimate connection between the tricarboxylic acid (TCA) cycle and c-di-GMP signaling for controlling virulence. Using genome-wide transposon mutagenesis, we uncover a group of transposon insertion mutants affecting several TCA cycle enzymes recovers the c-di-GMP-mediated repression on swimming motility. Chromosomal deletion of two selected TCA cycle enzyme encoding genes or operon, fumA gene (encoding fumarase) and sdhCDAB operon (encoding succinate dehydrogenase), validates the transposon mutagenesis data and exhibits enhanced production of pectate lyases (Pels), a major plant-cell-wall degrading enzyme (PCWDE) that is known to be repressed by c-di-GMP. A positive correlation between the TCA cycle and c-di-GMP signaling is established: deletion of sdhCDAB operon shows an imbalanced TCA cycle and reduces intracellular concentrations of c-di-GMP, whereas addition of citrate, a TCA intermediate, increases the intracellular c-di-GMP levels. Further study shows that protein levels of a c-di-GMP-producing diguanylate cyclase (DGC), GcpA, and a c-di-GMP-degrading phosphodiesterase (PDE), EGcpB, are induced and repressed respectively by the addition of citrate. GcpA and EGcpB have been reported to function as a DGC and PDE couple that controls Pel via the global post-transcriptional regulatory system, RsmA/RsmB. In summary, our report proposes a novel signaling cascade that links bacterial respiration metabolism with secondary messenger metabolism for controlling virulence.