Transcriptome of an entomophthoralean fungus (Pandora formicae) shows molecular machinery adjusted for successful host exploitation and transmission
Joanna Małagocka1, Morten N Grell2, Lene Lange2
1Centre for Social Evolution, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark.
Abstract:
Pandora formicae is an obligate entomopathogenic fungus from the phylum Entomophthoromycota, known to infect only ants from the genus Formica. In the final stages of infection, the fungus induces the so-called summit disease syndrome, manipulating the host to climb up vegetation prior to death and fixing the dead cadaver to the surface, all to increase efficient spore dispersal. To investigate this fascinating pathogen-host interaction, we constructed interaction transcriptome libraries from two final infection stages from the material sampled in the field: (1) when the cadavers were fixed, but the fungus had not grown out through the cuticle and (2) when the fungus was growing out from host cadaver and producing spores. These phases mark the switch from within-host growth to reproduction on the host surface, after fungus outgrowth through host integument. In this first de novo transcriptome of an entomophthoralean fungus, we detected expression of many pathogenicity-related genes, including secreted hydrolytic enzymes and genes related to morphological reorganization and nutrition uptake. Differences in expression of genes in these two infection phases were compared and showed a switch in enzyme expression related to either cuticle breakdown or cell proliferation and cell wall remodeling, particularly in subtilisin-like serine protease and trypsin-like protease transcripts.
Insights
Pandora formicae, an ant-infecting fungus, manipulates host behavior for spore dispersal. Transcriptome analysis reveals gene expression shifts during infection, from host invasion to spore production.
Area of Science:
- Entomopathogenic Mycology
- Insect Pathology
- Fungal Genomics
Background:
- Pandora formicae is an obligate entomopathogenic fungus infecting ants of the genus Formica.
- The fungus induces 'summit disease,' compelling hosts to climb vegetation before death for optimized spore dispersal.
Purpose of the Study:
- To investigate the molecular mechanisms underlying the Pandora formicae-Formica ant interaction.
- To analyze gene expression changes during the critical transition from host cadaver colonization to extracellular spore production.
Main Methods:
- Construction of interaction transcriptome libraries from field-sampled infected ants at two distinct late infection stages.
- De novo transcriptome sequencing and comparative analysis of gene expression profiles between the two stages.
Main Results:
- Detection of numerous pathogenicity-related genes, including secreted hydrolytic enzymes and genes for nutrient uptake and morphological changes.
- Identification of significant differences in gene expression between the two stages, highlighting a switch in enzyme activity.
- Observed differential expression of proteases (subtilisin-like serine proteases and trypsin-like proteases) linked to cuticle degradation and fungal proliferation.
Conclusions:
- The study provides the first de novo transcriptome of an entomophthoralean fungus, Pandora formicae.
- Gene expression analysis reveals a dynamic molecular strategy employed by the fungus during host manipulation and reproduction.
- The findings offer insights into the evolution of pathogenicity and host-parasite interactions in entomopathogenic fungi.
