Abstract
Garlic plants (Allium sativum L.) produce antimicrobial compounds, such as diallyl thiosulfinate (allicin) and diallyl polysulfanes. Here, we investigated the transcriptome and protein S-thioallylomes under allicin and diallyl tetrasulfane (DAS4) exposure in the Gram-positive bacterium Bacillus subtilis. Allicin and DAS4 caused a similar thiol-specific oxidative stress response, protein and DNA damage as revealed by the induction of the OhrR, PerR, Spx, YodB, CatR, HypR, AdhR, HxlR, LexA, CymR, CtsR, and HrcA regulons in the transcriptome. At the proteome level, we identified, in total, 108 S-thioallylated proteins under allicin and/or DAS4 stress. The S-thioallylome includes enzymes involved in the biosynthesis of surfactin (SrfAA, SrfAB), amino acids (SerA, MetE, YxjG, YitJ, CysJ, GlnA, YwaA), nucleotides (PurB, PurC, PyrAB, GuaB), translation factors (EF-Tu, EF-Ts, EF-G), antioxidant enzymes (AhpC, MsrB), as well as redox-sensitive MarR/OhrR and DUF24-family regulators (OhrR, HypR, YodB, CatR). Growth phenotype analysis revealed that the low molecular weight thiol bacillithiol, as well as the OhrR, Spx, and HypR regulons, confer protection against allicin and DAS4 stress. Altogether, we show here that allicin and DAS4 cause a strong oxidative, disulfide and sulfur stress response in the transcriptome and widespread S-thioallylation of redox-sensitive proteins in B. subtilis. The results further reveal that allicin and polysulfanes have similar modes of actions and thiol-reactivities and modify a similar set of redox-sensitive proteins by S-thioallylation.
Highlights
Garlic (Allium sativum) has been historically used as a medicinal plant for the treatment of infectious diseases, such as tuberculosis, due to the production of volatile reactive sulfur compounds.The main thiol-reactive sulfur ingredient of garlic is the diallyl thiosulfinate, which acts as antimicrobial and inhibits the growth and survival of several important human pathogens, including multi-drug resistant bacteria, fungi, and parasites [1,2,3,4,5,6,7,8,9]
We analyzed the growth of B. subtilis wild type cells after treatment with allicin and diallyl tetrasulfide (DAS4) to determine sub-lethal concentrations
Priming of B. subtilis cells with 90 μM allicin resulted in protection against subsequent treatment with lethal 250 μM allicin, as shown by the faster growth recovery in primed cells compared to those treated with 250 μM allicin alone (Figure 1A)
Summary
Garlic (Allium sativum) has been historically used as a medicinal plant for the treatment of infectious diseases, such as tuberculosis, due to the production of volatile reactive sulfur compounds. The main thiol-reactive sulfur ingredient of garlic is the diallyl thiosulfinate (allicin), which acts as antimicrobial and inhibits the growth and survival of several important human pathogens, including multi-drug resistant bacteria, fungi, and parasites [1,2,3,4,5,6,7,8,9]. The enzyme cysteine-S-lyase alliinase is released from the vacuole into the cytosol to synthesize allyl sulfenic acid and dehydroalanine from the odor-less precursor alliin. Allicin forms by spontaneous condensation of two allyl sulfenic acid molecules [5,10,11]. DAS2 and DAS3 are the most frequently observed sulfur compounds present in garlic oils [12,13,14]
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