Further evidences of an emerging stingless bee-yeast symbiosis

Gabriela Toninato de Paula; Weilan Gomes da Paixão Melo; Ivan de Castro; Cristiano Menezes; Camila Raquel Paludo; Carlos Augusto Rosa; Mônica Tallarico Pupo

doi:10.3389/fmicb.2023.1221724

Further evidences of an emerging stingless bee-yeast symbiosis

Front Microbiol. 2023 Aug 11:14:1221724. doi: 10.3389/fmicb.2023.1221724. eCollection 2023.

Authors

Gabriela Toninato de Paula¹, Weilan Gomes da Paixão Melo^{1

2}, Ivan de Castro³, Cristiano Menezes⁴, Camila Raquel Paludo⁵, Carlos Augusto Rosa⁶, Mônica Tallarico Pupo¹

Affiliations

¹ Department of Pharmaceutical Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil.
² Center for Agricultural and Natural Sciences and Letters, State University of the Tocantina Region of Maranhão, Estreito, Brazil.
³ Department of Genetics, Faculty of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil.
⁴ Brazilian Agricultural Research Corporation, Jaguariúna, Brazil.
⁵ Institute of Biological and Health Sciences, Federal University of Mato Grosso, Barra do Garças, Brazil.
⁶ Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.

Abstract

Symbiotic interactions between microorganisms and social insects have been described as crucial for the maintenance of these multitrophic systems, as observed for the stingless bee Scaptotrigona depilis and the yeast Zygosaccharomyces sp. SDBC30G1. The larvae of S. depilis ingest fungal filaments of Zygosaccharomyces sp. SDBC30G1 to obtain ergosterol, which is the precursor for the biosynthesis of ecdysteroids that modulate insect metamorphosis. In this work, we find a similar insect-microbe interaction in other species of stingless bees. We analyzed brood cell samples from 19 species of stingless bees collected in Brazil. The osmophilic yeast Zygosaccharomyces spp. was isolated from eight bee species, namely Scaptotrigona bipunctata, S. postica, S. tubiba, Tetragona clavipes, Melipona quadrifasciata, M. fasciculata, M. bicolor, and Partamona helleri. These yeasts form pseudohyphae and also accumulate ergosterol in lipid droplets, similar to the pattern observed for S. depilis. The phylogenetic analyses including various Zygosaccharomyces revealed that strains isolated from the brood cells formed a branch separated from the previously described Zygosaccharomyces species, suggesting that they are new species of this genus and reinforcing the symbiotic interaction with the host insects.

Keywords: Zygosaccharomyces; brood cell; fungi; stingless bees; symbiosis; yeast.

Grants and funding

This research was supported by the São Paulo Research Foundation (FAPESP) grants #2013/50954-0 (MP), #2013/07600-3 (MP; CEPID-CIBFar), #2018/03650-0 (GP), #2015/01001-6 (WM), by the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq) grants #303792/2018-2 and #307893/2022-7 (MP); #408733/2021-7 and #406564/2022-1 (CR), and by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) grant APQ-01525-14 (CR). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES)–Finance Code 001.