Abstract
Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D. flagrans encodes more than 100 of such putative SSPs one of which is the cysteine-rich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA-deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C. elegans reduced its lifespan. CyrA accumulated in C. elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.
Highlights
Nematode-trapping fungi (NTF) are carnivorous microorganisms that can trap and digest nematodes with sophisticated trapping structures
Pathogenic microorganisms are living at the expense of their host organisms and immediate killing of the host may be disadvantageous
Many bacterial or fungal pathogens developed an arsenal of small-secreted proteins during the colonization to modulate their host for instance to suppress its defense reactions
Summary
Nematode-trapping fungi (NTF) are carnivorous microorganisms that can trap and digest nematodes with sophisticated trapping structures. Nematode eggs are spread onto the pasture with the feces where they go through their life cycle and are re-ingested during grazing leading to re-infection This vicious cycle can be broken by feeding pellets containing NTF spores to the animals [2,9]. Duddingtonia flagrans is well suited for such an application because it produces robust and resistant chlamydospores besides adhesive, three-dimensional trapping networks [10,11,12] It has already been established successfully as a biocontrol agent in horses, cattle and other animals [13,14]. The chlamydospores survive the passage through the gastrointestinal tract and are able to germinate in the feces where they reduce the number of nematodes The genome of this fungus has been sequenced and annotated recently, and molecular and cell biological methods were developed [15]. This opens new avenues for basic research but may help to optimize the fungus as biocontrol agent
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