Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon

Abstract

Dead sporulating female fly cadavers infected by the house fly-pathogenic fungus Entomophthora muscae are attractive to healthy male flies, which by their physical inspection may mechanically trigger spore release and by their movement create whirlwind airflows that covers them in infectious conidia. The fungal artillery of E. muscae protrudes outward from the fly cadaver, and consists of a plethora of micrometric stalks that each uses a liquid-based turgor pressure build-up to eject a jet of protoplasm and the initially attached spore. The biophysical processes that regulate the release and range of spores, however, are unknown. To study the physics of ejection, we design a biomimetic ‘soft cannon’ that consists of a millimetric elastomeric barrel filled with fluid and plugged with a projectile. We precisely control the maximum pressure leading up to the ejection, and study the cannon efficiency as a function of its geometry and wall elasticity. In particular, we predict that ejection velocity decreases with spore size. The calculated flight trajectories under aerodynamic drag predict that the minimum spore size required to traverse a quiescent layer of a few millimetres around the fly cadaver is approximately 10 µm. This corroborates with the natural size of E. muscae conidia (approx. 27 µm) being large enough to traverse the boundary layer but small enough (less than 40 µm) to be lifted by air currents. Based on this understanding, we show how the fungal spores are able to reach a new host.

The genus Entomophthora: bringing the insect destroyers into the twenty-first century

“…Though there was once disagreement regarding the ejection mechanism of E. muscae primary conidia from conidiophores, recent work has conclusively demonstrated that primary conidia are fired using a water cannon mechanism (de Ruiter et al 2019 ). Each primary conidium is surrounded by a characteristic “halo” of material when landed on a surface.…”

Thermal robustness of biomechanical processes

“…Elastic recoil is often studied in animals where muscles load energy into springs, but diverse ectothermic organisms, from cnidarians to plants and fungi, use rapid release of energy that was stored slowly in tissues or fluid to fire nematocysts, seeds and spores, respectively, or to capture prey (Berg et al, 2019;de Ruiter et al, 2019;Edwards et al, 2005;Hayashi et al, 2010;Holstein and Tardent, 1984;Poppinga et al, 2016;Vincent et al, 2011). In cases where muscle cannot be described as a default motor for comparison, temperature effects on alternative physiological motors can be used to assess thermal robustness.…”

A pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

“…The entomopathogenic fungus, Entomophthora muscae, represents a unique example in that it not only behaviourally manipulates its immediate house fly (Musca domestica) host, but also appears to manipulate uninfected conspecifics. Prior to death, infected house flies are manipulated to seek out elevated positions and die with wings spread out in a specific posture conducive for active discharge of infectious fungal conidia, which occurs primarily within the first 24 hours post mortem (De Ruiter et al, 2019;Lovett et al, 2020). Male and female flies in the vicinity may become infected from being directly hit by a conidium (spore) or via contact with already-discharged conidia that form a halo on the surface surrounding a conidia-shooting cadaver (De Ruiter et al, 2019).…”