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 PathogenDickeya dadantii
Year: 2019
Type: article
Abstract: 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 Δhfq 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.
Institutions: Jiangsu Academy of Agricultural Sciences, University of Wisconsin–Milwaukee, Connecticut Agricultural Experiment Station, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Michigan State University, Zhejiang A & F University, Agricultural Research Service, United States Department of Agriculture, U.S. Salinity Laboratory
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
Funders: U.S. Department of Agriculture, University of Wisconsin-Milwaukee, Jiangsu Academy of Agricultural Sciences, National Institutes of Health, National Institute of Food and Agriculture, Earmarked Fund for China Agriculture Research System, National Institute of General Medical Sciences, National Institute of Allergy and Infectious Diseases
Awards: G18321624, G186283041, G2584419516, G3530432981, Developing novel technologies to address fundamental questions about second messenger signaling, From structure to systems: Understanding cyclic di-GMP control of transcription, Uncovering the first 5'-pGpG signaling system, G724698049, G7263336931
OpenAlex ID: W2995207680