Larvae of the parasitoid wasp Ampulex compressa sanitize their host, the American cockroach, with a blend of antimicrobials

Abstract

Food resources contaminated with spoilage or pathogenic microorganisms pose severe problems to all higher organisms. Here, we describe a food-hygienic strategy of the emerald cockroach wasp Ampulex compressa . The wasp larvae develop on and inside the American cockroach Periplaneta americana , a host that can harbor various putrefactive microbes, as well as human and insect pathogens. From P. americana , we isolated the Gram-negative bacterium Serratia marcescens , which is a potent entomopathogen that can rapidly kill insect larvae. It is also known as a food contaminant and as an opportunistic human pathogen. Using behavioral observations and chemical analyses, we demonstrated that A. compressa larvae impregnate their cockroach hosts from inside with large amounts of an oral secretion containing a blend of γ-lactones and isocoumarins with ( R )-(-)-mellein [( R )-(-)-3,4-diydro-8-hydroxy-3-methylisocoumarin] and micromolide [(4 R ,9 Z )-octadec-9-en-4-olide] as dominant components. We fractionated hexane extracts of the secretion and investigated the antimicrobial properties of the fraction containing the lactones and isocoumarins, as well as of synthetic ( R )-(-)-mellein and micromolide, against S. marcescens and a Gram-positive bacterium, Staphylococcus hyicus , in broth microdilution assays. The test fraction inhibited growth of both tested bacteria. The activity of the fraction against S. marcescens was explained by ( R )-(-)-mellein alone, and the activity against S. hyicus was explained by the combined action of ( R )-(-)-mellein and micromolide. Our data suggest that the specific combination of antimicrobials in the larval secretion provides an effective frontline defense against the unpredictable spectrum of microbes that A. compressa larvae may encounter during their development inside their cockroach hosts.

Solid Phase Micro-extraction (SPME) with In Situ Transesterification: An Easy Method for the Detection of Non-volatile Fatty Acid Derivatives on the Insect Cuticle

“…Periplaneta americana (PA) were obtained from laboratory populations kept at the University of Regensburg. They were reared under conditions described by Herzner et al (2013). Adult female cockroaches were frozen and stored at −23°C.…”

An In Planta -Expressed Polyketide Synthase Produces ( R )-Mellein in the Wheat Pathogen Parastagonospora nodorum

“…(R)-Mellein has also been shown to exhibit antiviral activity against hepatitis C virus (64), antiparasitic activity against Schistosoma mansoni (59), and zootoxicity against Artemia salina larvae (54). It has been reported to be a trail pheromone of ants (61,63), while the larvae of the parasitoid wasp Ampulex compressa apparently impregnate the cockroach host with (R)-mellein as one of the antimicrobials for defense against entomopathogenic microbes (62). Above all, the most commonly reported bioactivity of mellein and its derivatives is their non-host-specific toxicity against plants.…”

“…Despite the widespread occurrence of mellein in fungi, this is the first time that a fungal PKS gene responsible for the synthesis of mellein has been identified. Outside of the fungal kingdom, mellein has been found in actinomycetes (33) and insects (61)(62)(63).…”

Multifaceted Defense against Antagonistic Microbes in Developing Offspring of the Parasitoid Wasp Ampulex compressa (Hymenoptera, Ampulicidae)

“…This secretion comprises the two major components ( R )-(-)-mellein [( R )-(-)-3,4-diydro-8-hydroxy-3-methylisocoumarin; „mellein“ in the following] and micromolide [(4 R ,9 Z )-octadec-9-en-4-olide], as well as seven structurally related minor compounds. The isocoumarin mellein and the γ-lactone micromolide have been shown to be inhibitory towards a broad spectrum of bacteria, mycobacteria, fungi and a virus [1], [39], [40], [41], [42], [43], [44], [45]. Several of the minor compounds of the larval secretion, namely ( R )-octadecan-4-olide, 7-hydroxymellein, 4-hydroxymellein, and 5-hydroxymellein [1] also seem to have broad antimicrobial activity [44], [45], [46], [47], [48].…”

“…The isocoumarin mellein and the γ-lactone micromolide have been shown to be inhibitory towards a broad spectrum of bacteria, mycobacteria, fungi and a virus [1], [39], [40], [41], [42], [43], [44], [45]. Several of the minor compounds of the larval secretion, namely ( R )-octadecan-4-olide, 7-hydroxymellein, 4-hydroxymellein, and 5-hydroxymellein [1] also seem to have broad antimicrobial activity [44], [45], [46], [47], [48]. The ultimate evolutionary and ecological function of this blend of compounds thus seems to be the protection of the larval food from an unpredictable array of competing, putrefactive microbes and of the A. compressa offspring themselves from pathogens.…”