Polaramycin B, and not physical interaction, is the signal that rewires fungal metabolism in the Streptomyces-Aspergillus interaction

Environ Microbiol. 2022 Oct;24(10):4899-4914. doi: 10.1111/1462-2920.16118. Epub 2022 Jul 18.

Abstract

Co-culturing the bacterium Streptomyces rapamycinicus and the ascomycete Aspergillus nidulans has previously been shown to trigger the production of orsellinic acid (ORS) and its derivates in the fungal cells. Based on these studies it was assumed that direct physical contact is a prerequisite for the metabolic reaction that involves a fungal amino acid starvation response and activating chromatin modifications at the biosynthetic gene cluster (BGC). Here we show that not physical contact, but a guanidine containing macrolide, named polaramycin B, triggers the response. The substance is produced constitutively by the bacterium and above a certain concentration, provokes the production of ORS. In addition, several other secondary metabolites were induced by polaramycin B. Our genome-wide transcriptome analysis showed that polaramycin B treatment causes downregulation of fungal genes necessary for membrane stability, general metabolism and growth. A compensatory genetic response can be observed in the fungus that included upregulation of BGCs and genes necessary for ribosome biogenesis, translation and membrane stability. Our work discovered a novel chemical communication, in which the antifungal bacterial metabolite polaramycin B leads to the production of antibacterial defence chemicals and to the upregulation of genes necessary to compensate for the cellular damage caused by polaramycin B.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / metabolism
  • Anti-Bacterial Agents / pharmacology
  • Antifungal Agents / metabolism
  • Aspergillus nidulans* / genetics
  • Aspergillus nidulans* / metabolism
  • Chromatin / metabolism
  • Electrolytes
  • Guanidines
  • Macrolides / metabolism
  • Multigene Family
  • Resorcinols
  • Secondary Metabolism / genetics
  • Streptomyces* / genetics
  • Streptomyces* / metabolism

Substances

  • Amino Acids
  • Anti-Bacterial Agents
  • Antifungal Agents
  • Chromatin
  • Electrolytes
  • Guanidines
  • Macrolides
  • orsellinic acid
  • polaramycin B
  • Resorcinols