Fungal Pathogens of Insects: Cuticle Degrading Enzymes and Toxins

Pathogenic fungi are important natural regulators of insect populations. However, many attempts to harness their potential for pest control have met with comparatively minor commercial success. Studies on mechanisms of pathogenesis have yet to contribute to the development of more efficient mycoinsecticides, but new insights into the pathogenic process are laying the groundwork. Significant progress has been made in particular in understanding enzymes involved with the penetration of host cuticle and the role of insecticidal toxins. Insect cuticle comprises up to 70% protein and it is not surprising that extracellular fungal proteases appear to be particularly important in the penetration process. Subtilisins, chymotrypsins, trypsins and metalloproteases, usually with multiple isoforms of each, provide an impressive backed-up arsenal. Pathogenic fungi produce a wide variety of toxic metabolites, which vary from low molecular weight products of secondary metabolism to complex cyclic peptides and proteolytic enzymes. Comparatively few compounds have been found in diseased insects, in quantities sufficient to account for symptoms of mycosis. An exception, a family of cyclic peptides called the destruxins, are dealt with in detail. The potential for synergy between toxins is explored also. I. I N T R O D U C T I O N Insect fungal pathogens hold a special place in the study of microbial pathogenesis. Agostino Bassi's monograph in 1835 established for the first time that a microorganism (the fungus later to be called Beauveria bassiana in Bassi's honour) could cause an infectious disease in an animal (the silkworm, Bornbyx mori) (see Fig. 1). Prophetic~rlly Bassi suggested further that microbes could be used to control pest insects (Bassi, 1835). Natural epizootics of insect fungal diseases are comparatively common, and their impact on insect populations further demonstrates the potential of microbial pest control (Carruthers and Soper, 1987). This fact was recognised in the latter part of the 19th century and culminated in the seminal attempts by Metchnikoff and Paliokov to use the Deuteromycotina fungal pathogen Metarhiziurn anisopliae for insect control (Gillespie, 1988). Despite these and other early successes, synthetic chemical pesticides have been the mainstay of insect pest control for the last 50 years. However, the advent of insecticide resistance and concern over the environmental impact of agricultural inputs focus attention on biologically based forms of pest control. Mycoinsecticides have a toe-hold in a biological crop protection market (see e.g. Fig. lc) dominated by the toxins from Bacillus thuringiensis (Bt) and crop plants transformed with Bt delta endotoxin genes (Charnley, 1997). FUNGAL PATHOGENS OF INSECTS 243