PMID- 31851880 OWN - NLM STAT- MEDLINE DCOM- 20200302 LR - 20220916 IS - 0894-0282 (Print) IS - 0894-0282 (Linking) VI - 33 IP - 2 DP - 2020 Feb TI - 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. PG - 296-307 LID - 10.1094/MPMI-07-19-0203-R [doi] AB - Dickeya dadantii is a plant-pathogenic bacterium that causes soft-rot in a wide range of plants. Although we have previously demonstrated that cyclic bis-(3'-5')-cyclic dimeric guanosine monophosphate (c-di-GMP), a bacterial secondary messenger, plays a central role in virulence regulation in D. dadantii, the upstream signals that modulate c-di-GMP remain enigmatic. Using a genome-wide transposon mutagenesis approach of a Deltahfq mutant strain that has high c-di-GMP and reduced motility, we uncovered transposon mutants that recovered the c-di-GMP-mediated repression on swimming motility. A number of these mutants harbored transposon insertions in genes encoding tricarboxylic acid (TCA) cycle enzymes. Two of these TCA transposon mutants were studied further by generating chromosomal deletions of the fumA gene (encoding fumarase) and the sdhCDAB operon (encoding succinate dehydrogenase). Disruption of the TCA cycle in these deletion mutants resulted in reduced intracellular c-di-GMP and enhanced production of pectate lyases (Pels), a major plant cell wall-degrading enzyme (PCWDE) known to be transcriptionally repressed by c-di-GMP. Consistent with this result, addition of TCA cycle intermediates such as citrate also resulted in increased c-di-GMP levels and decreased production of Pels. Additionally, we found that a diguanylate cyclase GcpA was solely responsible for the observed citrate-mediated modulation of c-di-GMP. Finally, we demonstrated that addition of citrate induced not only an overproduction of GcpA protein but also a concomitant repression of the c-di-GMP-degrading phosphodiesterase EGcpB which, together, resulted in an increase in the intracellular concentration of c-di-GMP. In summary, our report demonstrates that bacterial respiration and respiration metabolites serve as signals for the regulation of c-di-GMP signaling. FAU - Yuan, Xiaochen AU - Yuan X AD - Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of Ministry of Science and Technology, Nanjing, 210014, China. AD - Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI 53211, U.S.A. FAU - Zeng, Quan AU - Zeng Q AD - Department of Plant Pathology and Ecology, The Connecticut Agricultural Experiment Station, New Haven, CT 06511, U.S.A. FAU - Xu, Jingsheng AU - Xu J AD - Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China. FAU - Severin, Geoffrey B AU - Severin GB AD - Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, U.S.A. FAU - Zhou, Xiang AU - Zhou X AD - School of Forestry and Biotechnology, Zhejiang Agricultural and Forestry University, Hangzhou, 311300, China. FAU - Waters, Christopher M AU - Waters CM AD - Department of Microbiology and Molecular Genetics, Michigan State University. FAU - Sundin, George W AU - Sundin GW AD - Department of Plant, Soil, and Microbial Sciences, Michigan State University. FAU - Ibekwe, Abasiofiok M AU - Ibekwe AM AD - Agricultural Research Service-US Salinity Laboratory, United States Department of Agriculture, Riverside, CA 92507, U.S.A. FAU - Liu, Fengquan AU - Liu F AD - Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of Ministry of Science and Technology, Nanjing, 210014, China. FAU - Yang, Ching-Hong AU - Yang CH AUID- ORCID: 0000-0001-5330-7055 AD - Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI 53211, U.S.A. LA - eng GR - R01 GM109259/GM/NIGMS NIH HHS/United States GR - R03 AI130554/AI/NIAID NIH HHS/United States GR - R21 AI144395/AI/NIAID NIH HHS/United States PT - Journal Article DEP - 20191218 PL - United States TA - Mol Plant Microbe Interact JT - Molecular plant-microbe interactions : MPMI JID - 9107902 RN - 0 (Bacterial Proteins) RN - 61093-23-0 (bis(3',5')-cyclic diguanylic acid) RN - H2D2X058MU (Cyclic GMP) RN - Dickeya dadantii SB - IM MH - *Bacterial Proteins/genetics/metabolism MH - Cell Wall/microbiology MH - Cyclic GMP/*analogs & derivatives/genetics/metabolism MH - Dickeya MH - *Gammaproteobacteria/enzymology/genetics MH - Gene Expression Regulation, Bacterial/genetics MH - Mutation PMC - PMC9354473 MID - NIHMS1822306 OTO - NOTNLM OT - Dickeya dadantii OT - TCA cycle OT - bacterial pathogenesis OT - c-di-GMP OT - cell wall OT - metabolism OT - pectate lyase OT - soft rot COIS- The author(s) declare no conflict of interest. EDAT- 2019/12/19 06:00 MHDA- 2020/03/03 06:00 PMCR- 2022/08/05 CRDT- 2019/12/19 06:00 PHST- 2019/12/19 06:00 [pubmed] PHST- 2020/03/03 06:00 [medline] PHST- 2019/12/19 06:00 [entrez] PHST- 2022/08/05 00:00 [pmc-release] AID - 10.1094/MPMI-07-19-0203-R [doi] PST - ppublish SO - Mol Plant Microbe Interact. 2020 Feb;33(2):296-307. doi: 10.1094/MPMI-07-19-0203-R. Epub 2019 Dec 18.