Stable Isotopic Labeling of Dimethylallyl Pyrophosphate (DMAPP) Reveals Compartmentalization of Isoprenoid Biosynthesis during Sporulation in Bacillus subtilis

二甲基烯丙基焦磷酸酯 (DMAPP) 的稳定同位素标记揭示了枯草芽孢杆菌孢子形成过程中异戊二烯生物合成的区室化

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Abstract

Isoprenoids are essential metabolites whose biosynthesis originates from two five-carbon (C(5)) isomers, isopentenyl pyrophosphate (IPP) and dimethylallyl pyrophosphate (DMAPP). Although these isomers serve as the core substrates for isoprenoid biosynthesis, tracking their independent incorporation into downstream metabolites is difficult due to the lack of available chemical tools. To address this issue, we have developed a cell-permeant, stable isotope-labeled analog of DMAPP that employs self-immolating esters to mask the β-phosphate, allowing for efficient cellular uptake and direct forward isotopic labeling of downstream products of DMAPP in Bacillus subtilis. We demonstrate that (13)C-labeled, ester-protected DMAPP ((13)C(3) SIE-DMAPP) achieves significant incorporation into menaquinone-7 (MK-7), regardless of inhibition of endogenous production of IPP and DMAPP. By knocking out isopentenyl pyrophosphate isomerase (IPPI) expression, we achieve specific (13)C isotopic labeling exclusively at DMAPP-derived positions of MK-7 and demonstrate that IPPI overexpression enables B. subtilis to utilize DMAPP as its sole isoprenoid source. Finally, we tracked DMAPP incorporation during the transition from vegetative growth to sporulation, revealing compartment-specific isotope labeling patterns that underscore the metabolic independence of isoprenoid metabolism in the mother cell and endospore during sporulation in B. subtilis. The introduction of this stable isotope-labeled DMAPP facilitates the tracking of DMAPP-derived metabolites in native biological contexts and opens new avenues for studying prenyl metabolism, terpene biosynthetic pathways, and the regulatory mechanisms governing cellular isoprenoid pools.

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