The entomopathogenic fungus Metarhizium robertsii communicates with the insect host Galleria mellonella during infection

Virulence. 2018 Jan 1;9(1):402-413. doi: 10.1080/21505594.2017.1405190.

Abstract

Parasitic fungi are the only pathogens that can infect insect hosts directly through their proteinaceous exoskeleton. Penetration of the cuticle requires the release of fungal enzymes, including proteinases, which act as virulence factors. Insects can sense fungal infections and activate innate immune responses, including the synthesis of antifungal peptides and proteinase inhibitors that neutralize the incoming proteinases. This well-studied host response is epigenetically regulated by histone acetylation/deacetylation. Here we show that entomopathogenic fungi can in turn sense the presence of insect-derived antifungal peptides and proteinase inhibitors, and respond by inducing the synthesis of chymotrypsin-like proteinases and metalloproteinases that degrade the host-derived defense molecules. The rapidity of this response is dependent on the virulence of the fungal strain. We confirmed the specificity of the pathogen response to host-derived defense molecules by LC/MS and RT-PCR analysis, and correlated this process with the epigenetic regulation of histone acetylation/deacetylation. This cascade of responses reveals that the coevolution of pathogens and hosts can involve a complex series of attacks and counterattacks based on communication between the invading fungal pathogen and its insect host. The resolution of this process determines whether or not pathogenesis is successful.

Keywords: Metarhizium robertsii; antifungal peptides; epigenetics; fungal pathogenesis; fungi; galleria mellonella; insects; protease inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antimicrobial Cationic Peptides / metabolism
  • Chromatography, Liquid
  • Epigenesis, Genetic
  • Fungal Proteins / metabolism
  • Host-Pathogen Interactions*
  • Lepidoptera / genetics
  • Lepidoptera / immunology
  • Lepidoptera / microbiology*
  • Metarhizium / growth & development*
  • Peptide Hydrolases / metabolism
  • Protease Inhibitors / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • Antimicrobial Cationic Peptides
  • Fungal Proteins
  • Protease Inhibitors
  • Peptide Hydrolases

Grant support

AV acknowledges funding provided by the German Research Foundation for the project “The role of epigenetics in host–parasite coevolution” (Grant number VI 219/3-1/ VI 219/3-2) which is embedded within the DFG Priority Program 1399 “Host–parasite coevolution – rapid reciprocal adaptations and its genetic basis”. We acknowledge generous funding by the Hessen State Ministry of Higher Education, Research and the Arts (HMWK) via the ‘LOEWE Center for Insect Biotechnology and Bioresources'.