Logistic growth of the host‐specific obligate insect pathogenic fungus Entomophthora muscae in house flies (Musca domestica)

Abstract

Insect pathogenic fungi (IPF) need to overcome the host immune system in order to sporulate and ensure transmission to new hosts. Some IPF produce immunosuppressive toxins, whereas others rely on rapid fungal proliferation to kill the host by sheer fungal mass, resulting in a trade‐off between allocating resources to toxin production and fungal proliferation. The obligate entomopathogenic fungus, Entomophthora muscae sensu stricto, is host specific to the common house fly, Musca domestica. E. muscae grows as protoplast cells without cell walls and is not known to produce toxins. Here, we assessed the growth of E. muscae, in vivo, using real‐time PCR to measure the amount of a single‐copy actin gene. We find that E. muscae exhibits S‐shaped logistic growth between time post‐exposure and the number of fungal nuclei. The results show that E. muscae initially grows exponentially inside the host until depletion of available nutrient sources signifies the ‘limiting capacity’ where after the host is killed. This growth pattern differs markedly from toxin‐producing IPF species of Metarhizium and Beauveria in which maximal (plateau) growth and sporulation do not occur until well after the death of the host.

Infection of Drosophila suzukii with the obligate insect-pathogenic fungus Entomophthora muscae

“…Nevertheless, infected SWD, similar to house flies, showed climbing and posturing of the abdomen with conidiospores growing out between the tergites and sclerites, to get actively discharged. In the natural housefly host, E. muscae disease development is characterized by initial exponential growth (Hansen and De Fine Licht 2017 ), immune avoidance by proliferating as protoplasts without cell walls (Latge et al 1988 ) and behavioural manipulation of hosts to enhance transmission at the final stages of infection (Roy et al 2006 ; Gryganskyi et al 2017 ). Although less synchronized in time-to-kill, the disease ontogeny and complex behavioural manipulation of E. muscae in SWD is similar to infections in housefly.…”

“…An advantageous attribute for application in pest control is that members of the E. muscae species complex are dipteran-specific, which in comparison with generalist pathogens implies a smaller range of susceptible non-target species. Intricate molecular interactions underlying host-specific adaptation of E. muscae have led to a more narrow host range as compared to generalist hypocrealean fungi such as M. robertsii and B. bassiana (De Fine Licht et al 2017 ; Hansen and De Fine Licht 2017 ).…”

“…Flies of SWD ( D. suzukii ) originated from a laboratory strain maintained at SLU, Alnarp on a cornmeal diet (Revadi et al 2015 ). Entomophthora muscae isolate hhdfl130914-01, that was originally obtained from a dead infected M. domestica collected in a cow byre near Slangerup, Sealand, Denmark (Hansen and De Fine Licht 2017 ), and is deposited in the insect-pathogenic fungal culture collection at Department of Plant and Environmental Sciences, University of Copenhagen (acc. no.…”

“…6–7 days, E. muscae takes over the behaviour of infected hosts and forces them to seek out elevated positions. The host is eventually killed in a characteristic posture with wings spread away from the abdomen, while E. muscae grows out through the intersegmental membranes in the abdomen where it releases infective conidia (Gryganskyi et al 2017 ; Hansen and De Fine Licht 2017 ). Entomophthora muscae causes natural epizootics in housefly populations (Kalsbeek et al 2001 ), and here we explored the infectivity of E. muscae towards SWD.…”

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

“…Most stages of the infection cycle of E. muscae have been studied intensively [21][22][23]: conidia (spores) germinate on the host surface and penetrate through the insect cuticle into the haemolymph; the fungus proliferates logistically as protoplast cells until all nutrients are depleted; hyphal bodies and hyphae with cell walls are formed just before the host dies; rigid-walled conidiophores (spore-bearing stalks) penetrate outwards through the intersegmental membranes in the fly's abdomen; a single conidium is formed at the tip of each conidiophore (figure 1a).…”