Abstract

The larval stage of the stingless bee Scaptotrigona depilis must consume a specific brood cell fungus in order to continue development. Here we show that this fungus is a member of the genus Zygosaccharomyces and provides essential steroid precursors to the developing bee. Insect pupation requires ecdysteroid hormones, and as insects cannot synthesize sterols de novo, they must obtain steroids in their diet. Larval in vitro culturing assays demonstrated that consuming ergosterol recapitulates the developmental effects on S. depilis as ingestion of Zygosaccharomyces sp. cells. Thus, we determined the molecular underpinning of this intimate mutualistic symbiosis. Phylogenetic analyses showed that similar cases of bee-Zygosaccharomyces symbiosis may exist. This unprecedented case of bee-fungus symbiosis driven by steroid requirement brings new perspectives regarding pollinator-microbiota interaction and preservation.

Highlights

  • Bees originated in the wasp family Crabronidae[1] during the Cretaceous (113–132 million years ago) when angiosperms became the dominant flowering plants on the planet, and bee ancestors became phytophagous[2]

  • We show that Zygosaccharomyces sp. is the fungus eaten by S. depilis larvae and that fungus consumption provides ergosterol to developing bees, allowing successful pupation

  • In an effort to further understand the S. depilis (Fig. 1a) larvae-fungus interaction, the microbial mass accumulating inside S. depilis brood cells (Fig. 1b,c), and which the larvae eat, was carefully collected and plated on Potato Dextrose Agar (PDA) and International Streptomyces Project medium number 2 (ISP-2) agar

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Summary

Fungal Steroid to Pupate

The larval stage of the stingless bee Scaptotrigona depilis must consume a specific brood cell fungus in order to continue development. Phylogenetic analyses showed that similar cases of bee-Zygosaccharomyces symbiosis may exist. This unprecedented case of bee-fungus symbiosis driven by steroid requirement brings new perspectives regarding pollinator-microbiota interaction and preservation. The stingless bee Scaptotrigona depilis (Hymenoptera: Apidae: Meliponini) has a fascinating life history, requiring the consumption of a specific brood fungus during larval stage. The discovery of the beneficial symbiosis between S. depilis and the brood cell fungus initiated an important change in our ongoing bee microbiota studies. Phylogenetic analyses showed that other cases of bee-Zygosaccharomyces association may exist, opening new perspectives regarding bee-microbe symbiosis

Results
Monascus ruber
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