Could insect phagocytic avoidance by entomogenous fungi have evolved via selection against soil amoeboid predators?

Abstract

The entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana are ubiquitously distributed in soils. As insect pathogens they adhere to the insect cuticle and penetrate through to the insect haemocoel using a variety of cuticle-hydrolysing enzymes. Once in the insect haemocoel they are able to survive and replicate within, and/or evade, phagocytic haemocyte cells circulating in the haemolymph. The mechanism by which these soil fungi acquire virulence factors for insect infection and insect immune avoidance is unknown. We hypothesize that insect phagocytic cell avoidance in M. anisopliae and B. bassiana is the consequence of a survival strategy against soil-inhabiting predatory amoebae. Microscopic examination, phagocytosis assays and amoeba mortality assays showed that these insect pathogenic fungi are phagocytosed by the soil amoeba Acanthamoeba castellanii and can survive and grow within the amoeba, resulting in amoeba death. Mammalian fungal and bacterial pathogens, such as Cryptococcus neoformans and Legionella pneumophila, respectively, show a remarkable overlap between survival against soil amoebae and survival against human macrophages. The insect immune system, particularly phagocytic haemocytes, is analogous to the mammalian macrophage. Our data suggest that the ability of the fungal insect pathogens M. anisopliae and B. bassiana to survive insect phagocytic haemocytes may be a consequence of adaptations that have evolved in order to avoid predation by soil amoebae.