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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Plant, Soil and Nutrition Research » Research » Publications at this Location » Publication #419750

Research Project: Biochemistry and Physiology of Crop Adaptation to Soil-Based Abiotic Stresses

Location: Plant, Soil and Nutrition Research

Title: The Bacillus subtilis yqgC-sodA operon protects magnesium-dependent enzymes by supporting manganese efflux

Author
item SACHLA, ANKITA - Cornell University
item SONI, VIJAY - Cornell University
item Pineros, Miguel
item LOU, YUANCHAN - East China University Of Science And Technology
item IM, JANICE - Cornell University
item RHEE, KYU - Cornell University
item HELMANN, JOHN - Cornell University

Submitted to: Journal of Bacteriology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/8/2024
Publication Date: 5/31/2024
Citation: Sachla, A., Soni, V., Pineros, M., Lou, Y., Im, J., Rhee, K., Helmann, J. 2024. The Bacillus subtilis yqgC-sodA operon protects magnesium-dependent enzymes by supporting manganese efflux. Journal of Bacteriology. vol 206 (6): e00052-24. https://doi.org/10.1128/jb.00052-24.
DOI: https://doi.org/10.1128/jb.00052-24

Interpretive Summary: As bacteria require multiple trace metal ions for survival, their transport is the tightly regulated to minimize metal intoxication. Intoxication results when metal homeostasis is perturbed, quite often due to enzyme mis-metalation. The Mn-dependent superoxide dismutase (MnSOD) is the most abundant Mn-containing protein and is important, and usually associated with resistance to oxidative stress resistance. We have identified novel roles for MnSOD and the partner membrane protein YqgC, by examining how the loss of both these proteins affects Mn balance by prevents the efficient expression of Mn transport proteins. This inhibition leads to a large-scale perturbation of the cellular metabolite levels as a results of the inhibition of set of Mg-dependent enzymes. This information highlights and reveals novel pathways involved in maintaining a tight balance between avoiding intoxication whilst maintaining the uptake of essential, potentially toxic metals.

Technical Abstract: Microbes encounter a myriad of stresses during their life cycle. Dysregula tion of metal ion homeostasis is increasingly recognized as a key factor in host–microbe interactions. Bacterial metal ion homeostasis is tightly regulated by dedicated metallore gulators that control uptake, sequestration, trafficking, and efflux. Here, we demonstrate that deletion of the Bacillus subtilis yqgC-sodA (YS) complex operon, but not deletion of the individual genes, causes hypersensitivity to manganese (Mn). YqgC is an integral membrane protein of unknown function, and SodA is a Mn-dependent superoxide dismutase (MnSOD). The YS strain has reduced expression of two Mn efflux proteins, MneP and MneS, consistent with the observed Mn sensitivity. The YS strain accumulated high levels of Mn, had increased reactive radical species (RRS), and had broad metabolic alterations that can be partially explained by the inhibition of Mg-dependent enzymes. Although the YS operon deletion strain and an efflux-deficient mneP mneS double mutant both accumulate Mn and have similar metabolic perturbations, they also display phenotypic differences. Several mutations that suppressed Mn intoxication of the mneP mneS efflux mutant did not benefit the YS mutant. Further, Mn intoxication in the YS mutant, but not the mneP mneS strain, was alleviated by expression of Mg-dependent, chorismate-utilizing enzymes of the menaquinone, siderophore, and tryptophan (MST) family. Therefore, despite their phenotypic similarities, the Mn sensitivity in the mneP mneS and the YS deletion mutants results from distinct enzymatic vulnerabilities.