Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: hydrocarbon oxidation within the context of a host-pathogen interaction

Abstract

Broad host range entomopathogenic fungi such as Beauveria bassiana attack insect hosts via attachment to cuticular substrata and the production of enzymes for the degradation and penetration of insect cuticle. The outermost epicuticular layer consists of a complex mixture of non-polar lipids including hydrocarbons, fatty acids, and wax esters. Long chain hydrocarbons are major components of the outer waxy layer of diverse insect species, where they serve to protect against desiccation and microbial parasites, and as recognition molecules or as a platform for semiochemicals. Insect pathogenic fungi have evolved mechanisms for overcoming this barrier, likely with sets of lipid degrading enzymes with overlapping substrate specificities. Alkanes and fatty acids are substrates for a specific subset of fungal cytochrome P450 monooxygenases involved in insect hydrocarbon degradation. These enzymes activate alkanes by terminal oxidation to alcohols, which are further oxidized by alcohol and aldehyde dehydrogenases, whose products can enter β-oxidation pathways. B. bassiana contains at least 83 genes coding for cytochrome P450s (CYP), a subset of which are involved in hydrocarbon oxidation, and several of which represent new CYP subfamilies/families. Expression data indicated differential induction by alkanes and insect lipids and four CYP proteins have been partially characterized after heterologous expression in yeast. Gene knockouts revealed a phenotype for only one (cyp52X1) out of six genes examined to date. CYP52X1 oxidizes long chain fatty acids and participates in the degradation of specific epicuticular lipid components needed for breaching the insect waxy layer. Examining the hydrocarbon oxidizing CYP repertoire of pathogens involved in insect epicuticle degradation can lead to the characterization of enzymes with novel substrate specificities. Pathogen targeting may also represent an important co-evolutionary process regarding insect cuticular hydrocarbon synthesis.

Potential for entomopathogenic fungi to control Triatoma dimidiata (Hemiptera: Reduviidae), a vector of Chagas disease in Mexico

“…One important factor is the degradation and/or penetration of the initial barrier that must be overcome for successful infection to occur, particularly in relation to the hydrocarbons that constitute the insect epicuticle. The composition of surface lipids has profound consequences that affect the ecological and behavioral characteristics of insects 37 . However, it is more likely that low pathogenicity is an intrinsic characteristic of the fungal strain that we studied 27 .…”

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

“…Fungal spores (conidia) of the insect pathogenic fungus, B. bassiana, will attempt to attach and initiate infection essentially anywhere on host cuticle, although preferential infection sites on some hosts have been observed (21,49,50). The infection program is initiated by surface cues, and the fungus is capable of assimilating long-chain alkanes and other lipids that are often found as major constituents of the insect epicuticle (41). The subsequent production of cuticledegrading enzymes and penetrating hyphae results in growth of the fungus through the integument into the hemocoel.…”

“…However, entomopathogenic fungi are incapable of lignin degradation, and no information is available regarding the presence and/or function of these enzymes in this group of fungi. However, entomopathogenic fungi are able to assimilate various hydrocarbon and lipid components of the insect cuticle, responding to surface cues on their hosts to initiate programs for infection (41)(42)(43).…”

Expression of a Toll Signaling Regulator Serpin in a Mycoinsecticide for Increased Virulence

“…In some instances, when integrated with cuticular defenses, the insect immune system can recognize and attempt to eliminate invading microbes via a series of immune reactions that can include hemocyte activation and phagocytosis, encapsulation, melanization, and activation/expression of antimicrobial proteins and molecules (8,9). B. bassiana, however, has evolved mechanisms for overcoming these barriers that include secretion of cuticle-degrading enzymes, toxic metabolite production, mechanical penetration, and host immune evasion and suppression (35)(36)(37)(38). However, the length of time required to kill target insects and the high spore concentrations required have constrained the use of these fungi for insect control.…”