High sorbic acid resistance of Penicillium roqueforti is mediated by the SORBUS gene cluster

TY - JOUR

T1 - High sorbic acid resistance of Penicillium roqueforti is mediated by the SORBUS gene cluster

AU - Punt, Maarten

AU - Seekles, Sjoerd J

AU - van Dam, Jisca L

AU - de Adelhart Toorop, Connor

AU - Martina, Raithel R

AU - Houbraken, Jos

AU - Ram, Arthur F J

AU - Wösten, Han A B

AU - Ohm, Robin A

PY - 2022/6

Y1 - 2022/6

N2 - Penicillium roqueforti is a major food-spoilage fungus known for its high resistance to the food preservative sorbic acid. Here, we demonstrate that the minimum inhibitory concentration of undissociated sorbic acid (MICu) ranges between 4.2 and 21.2 mM when 34 P. roqueforti strains were grown on malt extract broth. A genome-wide association study revealed that the six most resistant strains contained the 180 kbp gene cluster SORBUS, which was absent in the other 28 strains. In addition, a SNP analysis revealed five genes outside the SORBUS cluster that may be linked to sorbic acid resistance. A partial SORBUS knock-out (>100 of 180 kbp) in a resistant strain reduced sorbic acid resistance to similar levels as observed in the sensitive strains. Whole genome transcriptome analysis revealed a small set of genes present in both resistant and sensitive P. roqueforti strains that were differentially expressed in the presence of the weak acid. These genes could explain why P. roqueforti is more resistant to sorbic acid when compared to other fungi, even in the absence of the SORBUS cluster. Together, the MICu of 21.2 mM makes P. roqueforti among the most sorbic acid-resistant fungi, if not the most resistant fungus, which is mediated by the SORBUS gene cluster.

AB - Penicillium roqueforti is a major food-spoilage fungus known for its high resistance to the food preservative sorbic acid. Here, we demonstrate that the minimum inhibitory concentration of undissociated sorbic acid (MICu) ranges between 4.2 and 21.2 mM when 34 P. roqueforti strains were grown on malt extract broth. A genome-wide association study revealed that the six most resistant strains contained the 180 kbp gene cluster SORBUS, which was absent in the other 28 strains. In addition, a SNP analysis revealed five genes outside the SORBUS cluster that may be linked to sorbic acid resistance. A partial SORBUS knock-out (>100 of 180 kbp) in a resistant strain reduced sorbic acid resistance to similar levels as observed in the sensitive strains. Whole genome transcriptome analysis revealed a small set of genes present in both resistant and sensitive P. roqueforti strains that were differentially expressed in the presence of the weak acid. These genes could explain why P. roqueforti is more resistant to sorbic acid when compared to other fungi, even in the absence of the SORBUS cluster. Together, the MICu of 21.2 mM makes P. roqueforti among the most sorbic acid-resistant fungi, if not the most resistant fungus, which is mediated by the SORBUS gene cluster.

KW - Fungi/genetics

KW - Genome-Wide Association Study

KW - Multigene Family

KW - Penicillium/genetics

KW - Sorbic Acid/pharmacology

KW - Sorbus/genetics

U2 - 10.1371/journal.pgen.1010086

DO - 10.1371/journal.pgen.1010086

M3 - Article

C2 - 35704633

SN - 1553-7404

VL - 18

SP - e1010086

JO - PLoS Genetics

JF - PLoS Genetics

IS - 6

ER -