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Temporal Changes in Gut Microbiota Composition and Pollen Diet Associated with Colony Weakness of a Stingless Bee

  • Invertebrate Microbiology
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Abstract

Compared to honeybees and bumblebees, the effect of diet on the gut microbiome of Neotropical corbiculate bees such as Melipona spp. is largely unknown. These bees have been managed for centuries, but recently an annual disease is affecting M. quadrifasciata, an endangered species kept exclusively by management in Southern Brazil. Here we report the results of a longitudinal metabarcoding study involving the period of M. quadrifasciata colony weakness, designed to monitor the gut microbiota and diet changes preceding an outbreak. We found increasing amounts of bacteria associated to the gut of forager bees 2 months before the first symptoms have been recorded. Simultaneously, forager bees showed decreasing body weight. The accelerated growth of gut-associated bacteria was uneven among taxa, with Bifidobacteriaceae dominating, and Lactobacillaceae decreasing in relative abundance within the bacterial community. Dominant fungi such as Candida and Starmerella also decreased in numbers, and the stingless bee obligate symbiont Zygosaccharomyces showed the lowest relative abundance during the outbreak period. Such changes were associated with pronounced diet shifts, i.e., the rise of Eucalyptus spp. pollen amount in forager bees’ guts. Furthermore, there was a negative correlation between the amount of Eucalyptus pollen in diets and the abundance of some bacterial taxa in the gut-associated microbiota. We conclude that diet and subsequent interactions with the gut microbiome are key environmental components of the annual disease and propose the use of diet supplementation as means to sustain the activity of stingless bee keeping as well as native bee pollination services.

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Data Availability

Sequencing data were deposited as a BioProject at NCBI under the accession PRJNA751106. Our R codes and datasets are available at https://github.com/klhaag/metabarcoding-melipona.

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Acknowledgements

We thank Evald Gossler and Aroni Sattler for making their meliponaries available for our study, and to Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul, Conselho Nacional de Desenvolvimento Científico e Tecnológico and Associação ABELHA for supporting our work. We are indebted to three anonymous reviewers for their important contributions to our manuscript.

Funding

This work was supported by Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul FAPERGS PQG 19/2551–0001860-6, Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq/MCTIC/IBAMA/Associação ABELHA #400597/2018–7, and CNPq PQ #302121/2017–0. LC was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Finance Code 001).

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Authors and Affiliations

  1. Department of Genetics and Program of Post Graduation in Genetics and Molecular Biology, Federal University of Rio Grande Do Sul, Porto Alegre, RS, Brazil

    Karen Luisa Haag, Lílian Caesar & Victor Montenegro Marcelino

  2. Department of Biology, Indiana University, Bloomington, IN, USA

    Lílian Caesar

  3. Department of Genetics, Federal University of Pernambuco, Recife, PE, Brazil

    Marcos da Silveira Regueira-Neto & Valdir de Queiroz Balbino

  4. Department of Agronomy and Program of Post Graduation in Entomology, Federal Rural University of Pernambuco, Recife, PA, Brazil

    Dayana Rosalina de Sousa

  5. Program of Post Graduation in Bioinformatics, Multidisciplinary Environment, Digital Metropolis Institute, Federal University of Rio Grande Do Norte, Natal, Brazil

    Victor Montenegro Marcelino

  6. Department of Biosciences, Center of Biological and Health Sciences, Federal Rural University of the Semi-Arid, Mossoró, RN, Brazil

    Airton Torres Carvalho

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  1. Karen Luisa Haag
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  2. Lílian Caesar
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  3. Marcos da Silveira Regueira-Neto
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  4. Dayana Rosalina de Sousa
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  5. Victor Montenegro Marcelino
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  6. Valdir de Queiroz Balbino
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  7. Airton Torres Carvalho
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Karen Luisa Haag, Lílian Caesar, Victor Montenegro Marcelino, Dayana Rosalina de Sousa, and Marcos da Silveira Regueira Neto. The first draft of the manuscript was written by Karen Luisa Haag and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Karen Luisa Haag.

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According to Brazilian law, samples were collected with permission ICMBIO MMA 66382–2 and the access to the genetic patrimony by the A1B8F1F SisGen register.

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The authors declare no competing interests.

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Haag, K.L., Caesar, L., da Silveira Regueira-Neto, M. et al. Temporal Changes in Gut Microbiota Composition and Pollen Diet Associated with Colony Weakness of a Stingless Bee. Microb Ecol 85, 1514–1526 (2023). https://doi.org/10.1007/s00248-022-02027-3

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