Abstract
Detrimental microbes caused the evolution of a great diversity of antimicrobial defenses in plants and animals. Insects developing underground seem particularly threatened. Here we show that the eggs of a solitary digger wasp, the European beewolf Philanthus triangulum, emit large amounts of gaseous nitric oxide (NO⋅) to protect themselves and their provisions, paralyzed honeybees, against mold fungi. We provide evidence that a NO-synthase (NOS) is involved in the generation of the extraordinary concentrations of nitrogen radicals in brood cells (~1500 ppm NO⋅ and its oxidation product NO2⋅). Sequencing of the beewolf NOS gene revealed no conspicuous differences to related species. However, due to alternative splicing, the NOS-mRNA in beewolf eggs lacks an exon near the regulatory domain. This preventive external application of high doses of NO⋅ by wasp eggs represents an evolutionary key innovation that adds a remarkable novel facet to the array of functions of the important biological effector NO⋅.
Highlights
Microbes pose a major threat to the health of all animals and plants
Employing bioassays we discovered that beewolf eggs emit a strong antifungal agent that we identified as the gaseous radical nitric oxide (NO.)
When one of the most abundant mold species from infested beewolf brood cells, the fast growing Aspergillus flavus [15], was exposed to the volatiles presumably emanating from beewolf eggs on nutrient agar for three days, its growth was entirely inhibited, whereas it thrived in controls
Summary
Microbes pose a major threat to the health of all animals and plants These have responded by 39 evolving a great diversity of defenses including hygienic behaviors [1], antimicrobial chemicals [240 4], complex immune systems [5,6], and defensive symbioses [7,8]. 54 Such hostile conditions prevail in nests of subsocial Hymenoptera like the European beewolf Philanthus triangulum (Hymenoptera, Crabronidae) The offspring of these solitary digger wasps develop in subterranean brood cells provisioned by the female wasps with paralyzed honeybee workers (Apis mellifera, Apidae, Hymenoptera) [14] (Fig. 1A). Without any countermeasures the provisions will be completely overgrown by mold fungi within three days (Fig. 1B), and the beewolf larva becomes infested by fungi or starves to death [16,17]
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