Production of Secondary Metabolites in Extreme Environments: Food- and Airborne Wallemia spp. Produce Toxic Metabolites at Hypersaline Conditions

PLoS One. 2016 Dec 30;11(12):e0169116. doi: 10.1371/journal.pone.0169116. eCollection 2016.

Abstract

The food- and airborne fungal genus Wallemia comprises seven xerophilic and halophilic species: W. sebi, W. mellicola, W. canadensis, W. tropicalis, W. muriae, W. hederae and W. ichthyophaga. All listed species are adapted to low water activity and can contaminate food preserved with high amounts of salt or sugar. In relation to food safety, the effect of high salt and sugar concentrations on the production of secondary metabolites by this toxigenic fungus was investigated. The secondary metabolite profiles of 30 strains of the listed species were examined using general growth media, known to support the production of secondary metabolites, supplemented with different concentrations of NaCl, glucose and MgCl2. In more than two hundred extracts approximately one hundred different compounds were detected using high-performance liquid chromatography-diode array detection (HPLC-DAD). Although the genome data analysis of W. mellicola (previously W. sebi sensu lato) and W. ichthyophaga revealed a low number of secondary metabolites clusters, a substantial number of secondary metabolites were detected at different conditions. Machine learning analysis of the obtained dataset showed that NaCl has higher influence on the production of secondary metabolites than other tested solutes. Mass spectrometric analysis of selected extracts revealed that NaCl in the medium affects the production of some compounds with substantial biological activities (wallimidione, walleminol, walleminone, UCA 1064-A and UCA 1064-B). In particular an increase in NaCl concentration from 5% to 15% in the growth media increased the production of the toxic metabolites wallimidione, walleminol and walleminone.

MeSH terms

  • Azasteroids / metabolism
  • Basidiomycota / classification
  • Basidiomycota / genetics*
  • Basidiomycota / metabolism*
  • Cholestadienols / metabolism
  • Chromatography, High Pressure Liquid
  • Extreme Environments*
  • Food Contamination
  • Food Microbiology
  • Glucose / metabolism
  • Magnesium Chloride / metabolism
  • Mycotoxins / metabolism*
  • Secondary Metabolism / genetics*
  • Secondary Metabolism / physiology
  • Sesquiterpenes / metabolism
  • Sodium Chloride / metabolism*

Substances

  • Azasteroids
  • Cholestadienols
  • Mycotoxins
  • Sesquiterpenes
  • walleminone
  • Magnesium Chloride
  • walleminol A
  • UCA 1064-B
  • Sodium Chloride
  • A25822B
  • Glucose

Grants and funding

The authors acknowledge the financial support from the Slovenian Research Agency to the Infrastructural Centre Mycosmo and for providing a Young Researcher Grant to SJ. The study was partly financed through the Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (Cipkebip, OP13.1.1.2.02.0005), which is financed by a European Regional Development Fund (85% share of financing) and by the Slovenian Ministry of Higher Education, Science and Technology (15% share of financing). The authors would like to acknowledge the support of the European Commission through the project MAESTRA - Learning from Massive, Incompletely annotated, and Structured Data (Grant number ICT-2013-612944). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.