Microbial community modulates growth of symbiotic fungus required for stingless bee metamorphosis

Camila Raquel Paludo,Cameron R Currie,Gleb Pishchany,Cristiano Menezes,Andres Andrade-Dominguez,Jon Clardy,Roberto Kolter,Eduardo Afonso Silva-Junior,Mônica Tallarico Pupo,Fabio Santos Nascimento,Kleber Del-Claro

doi:10.1371/journal.pone.0219696

Abstract

The Brazilian stingless bee Scaptotrigona depilis requires the brood cells-associated fungus Zygosaccharomyces sp. as steroid source for metamorphosis. Besides the presence of Zygosaccharomyces sp., other fungi inhabit S. depilis brood cells, but their biological functions are unknown. Here we show that Candida sp. and Monascus ruber, isolated from cerumen of S. depilis brood provisions, interact with Zygosaccharomyces sp. and modulate its growth. Candida sp. produces volatile organic compounds (VOCs) that stimulate Zygosacchromyces sp. development. Monascus ruber inhibits Zygosacchromyces sp. growth by producing lovastatin, which blocks steroid biosynthesis. We also observed that in co-cultures M. ruber inhibits Candida sp. through the production of monascin. The modulation of Zygosaccharomyces sp. growth by brood cell-associated fungi suggests their involvement in S. depilis larval development. This tripartite fungal community opens new perspectives in the research of microbial interactions with bees.

Highlights

The Brazilian stingless bee Scaptotrigona depilis (Moure, 1942) (Hymenoptera, Apidae, Meliponini) requires the fungus Zygosaccharomyces sp. to develop
The lack of information about the roles of the microbial communities isolated from stingless bees’ colonies prompted us to further study the microbiota associated with S. depilis brood cells
Our initial hypothesis was that Zygosaccharomyces sp., Monascus ruber and Candida sp., repeatedly isolated from brood cells of S. depilis, should interact among themselves via small molecules production

Summary

Introduction

The Brazilian stingless bee Scaptotrigona depilis (Moure, 1942) (Hymenoptera, Apidae, Meliponini) requires the fungus Zygosaccharomyces sp. to develop. The lack of information about the roles of the microbial communities isolated from stingless bees’ colonies prompted us to further study the microbiota associated with S. depilis brood cells. Our initial hypothesis was that Zygosaccharomyces sp., Monascus ruber and Candida sp., repeatedly isolated from brood cells of S. depilis, should interact among themselves via small molecules production. SDCP2 were isolated from S. depilis cerumen found in brood cells (S1 Fig).

Results

Conclusion