Distinct Transcriptional Changes in Response to Patulin Underlie Toxin Biosorption Differences in Saccharomyces cerevisiae

Abstract

Patulin (4-hydroxy-4H-furo[3,2c]pyran-2[6H]-one) is a mycotoxin produced by a suite of fungi species. Patulin is toxic to humans and is a sporadic contaminant in products that were made from fungi-infected fruits. The baker yeast Saccharomyces cerevisiae (S. cerevisiae) has been shown to decrease patulin levels likely by converting it to the less harmful E-ascladiol, yet this capacity is dependent on the strain utilized. In this study we show that four representative strains of different S. cerevisiae lineages differ in their ability to tolerate and decrease patulin levels in solution, demonstrating that some strains are better suitable for patulin biocontrol. Indeed, we tested the biocontrol capacities of the best patulin-reducer strain (WE) in contaminated apple juice and demonstrated their potential role as an efficient natural biocontrol solution. To investigate the mechanisms behind the differences between strains, we explored transcriptomic changes of the top (WE strain) and worst (WA strain) patulin-biocontroller strains after being exposed to this toxin. Large and significant gene expression differences were found between these two strains, the majority of which represented genes associated with protein biosynthesis, cell wall composition and redox homeostasis. Interestingly, the WE isolate exhibited an overrepresentation of up-regulated genes involved in membrane components, suggesting an active role of the membrane towards patulin detoxification. In contrast, WA upregulated genes were associated with RNA metabolism and ribosome biogenesis, suggesting a patulin impact upon transcription and translation activity. These results suggest that different genotypes of S. cerevisiae encounter different stresses from patulin toxicity and that different rates of detoxification of this toxin might be related with the plasma membrane composition. Altogether, our data demonstrates the different molecular mechanisms in S. cerevisiae strains withstanding patulin exposure and opens new avenues for the selection of new patulin biocontroller strains.

Biocontrol yeasts: mechanisms and applications

“…A number of S. cerevisiae strains (e.g., DISAABA1182, RC008, RC009, RC012, and RC016) reduced the growth of plant pathogens such as A. carbonarius , A. ochraceus , A. parasiticus or Fusarium graminearum and also inhibited mycotoxin (e.g., aflatoxin, ochratoxin A, zearalenone, deoxynivalenol) production by these species (Armando et al 2012a, 2013; Cubaiu et al 2012). The mycotoxin-removing activity is due to adsorption to S. cerevisiae cell walls, stress responses to the toxin (e.g., changes in plasma membrane composition following patulin exposure), as well as direct transcriptional downregulation of polyketide synthesis (Armando et al 2012b; Cubaiu et al 2012; Oporto et al 2019). Other biocontrol mechanisms employed by S. cerevisiae include the secretion of killer activity and hydrolytic enzymes as well as organic volatile compounds in yeasts that have been described and studied with respect to their antifungal activity against C. acutatum on citrus (Lopes et al 2015) (also see Supplementary Table 1).…”

Protection of Citrus Fruits from Postharvest Infection with Penicillium digitatum and Degradation of Patulin by Biocontrol Yeast Clavispora lusitaniae 146

“…C. lusitaniae degraded patulin as fast as R. paludigenum and much faster than S. cerevisiae . The efficiency of patulin degradation by S. cerevisiae varies among strains [ 44 , 45 ]. The S. cerevisiae strain used in this work degraded patulin with a substantially lower efficiency than C. lusitaniae and R. paludigenum.…”

Saccharomyces cerevisiae: Multifaceted Applications in One Health and the Achievement of Sustainable Development Goals

“…The harmful effects of food-borne mycotoxins on human health are considered a global health issue [29]. SC strains can effectively inhibit mycotoxigenic fungi growth and reduce mycotoxin levels [25,28] by adsorbing them in the cell wall and lowering polyketide and secondary metabolite production [25,26,[30][31][32].…”