The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis

Abstract

The observation that some aspects of amoeba-fungal interactions resemble animal phagocytic cell-fungal interactions, together with the finding that amoeba passage can enhance the virulence of some pathogenic fungi, has stimulated interest in the amoeba as a model system for the study of fungal virulence. Amoeba provide a relatively easy and cheap model system where multiple variables can be controlled for the study of fungi-protozoal (amoeba) interactions. Consequently, there have been significant efforts to study fungal–amoeba interactions in the laboratory, which have already provided new insights into the origin of fungal virulence as well as suggested new avenues for experimentation. In this essay we review the available literature, which highlights the varied nature of amoeba-fungal interactions and suggests some unsolved questions that are potential areas for future investigation. Overall, results from multiple independent groups support the ‘amoeboid predator–fungal animal virulence hypothesis’, which posits that fungal cell predation by amoeba can select for traits that also function during animal infection to promote their survival and thus contribute to virulence.

A hidden battle in the dirt: soil amoebae interactions withParacoccidioidesspp

“…These results suggest similarities between fungal molecules that are recognized by phagocytosis receptors in amoebae and mammals. Overall, our results fit into the recently formulated amoeboid predator-fungal animal virulence hypothesis whereby there is a nexus of causation from selective pressure of amoeboid environmental predators and the evolution of fungal virulence against mammals [13]. We have shown that Paracoccidioides spp.…”

“…Our results support the hypothesis that interaction with sympatric soil predators selects for traits that allow survival of Paracoccidioides spp. in mammalian hosts and add to the existing evidence for the amoeboid predator-animal virulence hypothesis [13].…”

Pseudomonas aeruginosaisolates co-incubated withAcanthamoeba castellaniiexhibit phenotypes similar to chronic cystic fibrosis isolates

“…Most opportunistic pathogens are not transmitted person to person but rather transit through the environment between hosts and therefore, it is likely that the environment plays a significant role in evolution of protective traits. Predation by protists is one of the major mortality factors for bacteria in the environment and it is likely that traits that protect against predation may also impact human hosts during infection (1–3). P. aeruginosa is responsible for a variety of nosocomial acute as well as chronic infections (15) in particular chronic lung infections in CF patients (16).…”

“…harm caused by a pathogen towards its host, is a long-standing subject of investigation with important implications for human health. Most opportunistic pathogens are not transmitted person to person but rather transit through the environment between hosts and therefore, it is unlikely that virulence traits evolve in the host (1–3). Rather, it is more likely that these traits evolve in the environment.…”

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

“…As opposed to most Candida species which have a long‐term history as human commensals, fungi such as A. fumigatus or Cr. neoformans reside in natural reservoirs suggesting that predatory selection pressure by amoebae and other protists could have driven the emergence of phagocytic escape mechanisms and thereby promote survival in mammalian hosts (Erken et al, ; Casadevall et al, ). Experimental studies have corroborated this idea using well‐known model organisms such as Dictyostelium discoideum or Acanthamoeba castellanii , showing that fungi can exploit their virulence determinants to escape phagocytic uptake or killing (Steenbergen et al, ; Steenbergen et al, ; Van Waeyenberghe et al, ; Hillmann et al, ; Koller et al, ; Novohradska et al, ).…”