AUTHOR=Palmieri Davide , Miccoli Cecilia , Notardonato Ivan , Avino Pasquale , Lima Giuseppe , De Curtis Filippo , Ianiri Giuseppe , Castoria Raffaello 

TITLE=Modulation of extracellular Penicillium expansum-driven acidification by Papiliotrema terrestris affects biosynthesis of patulin and has a possible role in biocontrol activity

JOURNAL=Frontiers in Microbiology

VOLUME=Volume 13 - 2022

YEAR=2022

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2022.973670

DOI=10.3389/fmicb.2022.973670

ISSN=1664-302X

ABSTRACT=The active regulation of extracellular pH is critical for the virulence of fungal pathogens. Penicillium expansum is the causal agent of green-blue mold on stored pome fruits and produces the mycotoxin patulin (PAT). This fungus acidifies the host tissue by secreting organic acids, thus fostering the infection process. PAT is a serious health hazard for the carcinogenic potential of contaminated pome fruit-based products. In recent years, nutritional factors such as carbon and nitrogen were shown to affect PAT biosynthesis. Conversely, few studies have investigated the consequences of biocontrol on the accumulation of mycotoxins by producer fungi. In this work, we assessed the effects of optimal and suboptimal concentrations of the biocontrol agent (BCA) Papiliotrema terrestris LS28 both on extracellular pH and on PAT biosynthesis. In wounded apples, the optimal and suboptimal concentrations of the BCA provided almost complete and partial protection from P. expansum infection, respectively, and reduced PAT contamination in both cases. However, the suboptimal concentration of the BCA increased the specific mycotoxigenic activity by P. expansum. In vitro, the rate of PAT biosynthesis was strictly related to the extracellular pH, with the highest amount of PAT detected in the pH range 4-7, whereas only traces were detectable at pH 3. Moreover, both in vitro and in apple wounds the BCA counteracted the extracellular P. expansum-driven acidification, maintaining extracellular pH at 4 for the entire duration of the experiments, i.e. within the pH range that is optimal for PAT biosynthesis. Conversely, in the absence of LS28 the pathogen-driven acidification led to rapidly achieving acidic pH values (<3) that lie outside of the optimal pH range for PAT biosynthesis. Taken together, these results suggest that pH modulation by LS28 is important to counteract the host tissue acidification and, therefore, the virulence of P. expansum. On the other hand, the buffering of P. expansum-driven acidification provided by the BCA increases the specific rate of PAT biosynthesis, through the extension of the time interval at which the pH value lies within the optimal range for PAT biosynthesis. Nevertheless, the antagonistic effect provided by the BCA greatly reduced the total amount of PAT.