Further evidences of an emerging stingless bee-yeast symbiosis

Abstract

AbstractSymbiotic interactions between microorganisms and social insects have been described as crucial for the maintenance of these multitrophic systems, as observed for the stingless beeScaptotrigona depilisand the yeastZygosaccharomycessp. The larvae ofS. depilisingest fungal filaments ofZygosaccharomycessp. to obtain ergosterol, which is the precursor for the biosynthesis of ecdysteroids that modulate insect metamorphosis. In this work we verified that nutritional fungal symbioses also occur in other species of stingless bees. We analyzed brood cell samples from 19 species of stingless bees collected in Brazil. The osmophilic yeastZygosaccharomycesspp. was isolated from eight bee species, namelyScaptotrigona bipuctata, S. postica, S. tubiba, Tetragona clavipes, Melipona quadrifasciata, M. fasciculata, M. bicolorandPartamona helleri. These yeasts form pseudohyphae and also accumulate ergosterol in lipid droplets, similar to the pattern observed forS. depilis. The phylogenetic analyses including variousZygosaccharomycesrevealed that strains isolated from the brood cells formed a branch separated from the previously describedZygosaccharomycesspecies, suggesting that they are new species of this genus and reinforcing the symbiotic interaction with the host insects.ImportanceBenefits exchanged in insect–fungus mutualisms include nutrition, protection, and dispersal. Fungal nutritional roles are well described for some eusocial insects, such as fungus growing ants and termites, but similar interaction in stingless bees was so far observed just inScaptotrigona depilis. Here we expand the knowledge of yeast-bee symbiosis by analyzing the presence, cell morphologies, lipid accumulation and phylogenetic relationships of fungi isolated from brood cells and other locations of bee colonies.Zygosaccharomycesisolates were recovered from 42% of the bee species assessed, and probably represent new species showing pseudohyphae formation and lipid accumulation similar toS. depilisassociatedZygosaccharomycesstrains. The phylogenetic analyses suggested an evolutionary adaptation ofZygosaccharomycesspp. to the brood cell environment to provide nutritional benefits for the developing insect. Stingless bees play important ecosystem services, and our results raise the concern that fungicidal agents used in agriculture could disrupt this symbiosis, impacting bee health.