Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees

ABSTRACT Social bees harbor conserved gut microbiotas that may have been acquired in a common ancestor of social bees and subsequently codiversified with their hosts. However, most of this knowledge is based on studies on the gut microbiotas of honey bees and bumblebees. Much less is known about the...

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Main Authors: Garance Sarton-Lohéac, Carlos Gustavo Nunes da Silva, Florent Mazel, Gilles Baud, Vincent de Bakker, Sudip Das, Yassine El Chazli, Kirsten Ellegaard, Marc Garcia-Garcera, Natasha Glover, Joanito Liberti, Lorena Nacif Marçal, Aiswarya Prasad, Vincent Somerville, Germán Bonilla-Rosso, Philipp Engel
Format: Article
Language:English
Published: American Society for Microbiology 2023-04-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.03538-22
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author Garance Sarton-Lohéac
Carlos Gustavo Nunes da Silva
Florent Mazel
Gilles Baud
Vincent de Bakker
Sudip Das
Yassine El Chazli
Kirsten Ellegaard
Marc Garcia-Garcera
Natasha Glover
Joanito Liberti
Lorena Nacif Marçal
Aiswarya Prasad
Vincent Somerville
Germán Bonilla-Rosso
Philipp Engel
author_facet Garance Sarton-Lohéac
Carlos Gustavo Nunes da Silva
Florent Mazel
Gilles Baud
Vincent de Bakker
Sudip Das
Yassine El Chazli
Kirsten Ellegaard
Marc Garcia-Garcera
Natasha Glover
Joanito Liberti
Lorena Nacif Marçal
Aiswarya Prasad
Vincent Somerville
Germán Bonilla-Rosso
Philipp Engel
author_sort Garance Sarton-Lohéac
collection DOAJ
description ABSTRACT Social bees harbor conserved gut microbiotas that may have been acquired in a common ancestor of social bees and subsequently codiversified with their hosts. However, most of this knowledge is based on studies on the gut microbiotas of honey bees and bumblebees. Much less is known about the gut microbiotas of the third and most diverse group of social bees, the stingless bees. Specifically, the absence of genomic data from their microbiotas presents an important knowledge gap in understanding the evolution and functional diversity of the social bee microbiota. Here, we combined community profiling with culturing and genome sequencing of gut bacteria from six neotropical stingless bee species from Brazil. Phylogenomic analyses show that most stingless bee gut isolates form deep-branching sister clades of core members of the honey bee and bumblebee gut microbiota with conserved functional capabilities, confirming the common ancestry and ecology of their microbiota. However, our bacterial phylogenies were not congruent with those of the host, indicating that the evolution of the social bee gut microbiota was not driven by strict codiversification but included host switches and independent symbiont gain and losses. Finally, as reported for the honey bee and bumblebee microbiotas, we found substantial genomic divergence among strains of stingless bee gut bacteria, suggesting adaptation to different host species and glycan niches. Our study offers first insights into the genomic diversity of the stingless bee microbiota and highlights the need for broader samplings to understand the evolution of the social bee gut microbiota. IMPORTANCE Stingless bees are the most diverse group of the corbiculate bees and represent important pollinator species throughout the tropics and subtropics. They harbor specialized microbial communities in their gut that are related to those found in honey bees and bumblebees and that are likely important for bee health. Few bacteria have been cultured from the gut of stingless bees, which has prevented characterization of their genomic diversity and functional potential. Here, we established cultures of major members of the gut microbiotas of six stingless bee species and sequenced their genomes. We found that most stingless bee isolates belong to novel bacterial species distantly related to those found in honey bees and bumblebees and encoding similar functional capabilities. Our study offers a new perspective on the evolution of the social bee gut microbiota and presents a basis for characterizing the symbiotic relationships between gut bacteria and stingless bees.
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spelling doaj.art-35bc8054ad2441778fedab3cf69c8d402023-04-25T13:04:57ZengAmerican Society for MicrobiologymBio2150-75112023-04-0114210.1128/mbio.03538-22Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless BeesGarance Sarton-Lohéac0Carlos Gustavo Nunes da Silva1Florent Mazel2Gilles Baud3Vincent de Bakker4Sudip Das5Yassine El Chazli6Kirsten Ellegaard7Marc Garcia-Garcera8Natasha Glover9Joanito Liberti10Lorena Nacif Marçal11Aiswarya Prasad12Vincent Somerville13Germán Bonilla-Rosso14Philipp Engel15Department of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Morphology, Instituto de Ciências Biológicas, Federal University of Amazonas, Manaus, BrazilDepartment of Ecology and Evolution, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandSociété des produits Nestlé, Lausanne, SwitzerlandSwiss Institute of Bioinformatics, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Morphology, Instituto de Ciências Biológicas, Federal University of Amazonas, Manaus, BrazilDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandABSTRACT Social bees harbor conserved gut microbiotas that may have been acquired in a common ancestor of social bees and subsequently codiversified with their hosts. However, most of this knowledge is based on studies on the gut microbiotas of honey bees and bumblebees. Much less is known about the gut microbiotas of the third and most diverse group of social bees, the stingless bees. Specifically, the absence of genomic data from their microbiotas presents an important knowledge gap in understanding the evolution and functional diversity of the social bee microbiota. Here, we combined community profiling with culturing and genome sequencing of gut bacteria from six neotropical stingless bee species from Brazil. Phylogenomic analyses show that most stingless bee gut isolates form deep-branching sister clades of core members of the honey bee and bumblebee gut microbiota with conserved functional capabilities, confirming the common ancestry and ecology of their microbiota. However, our bacterial phylogenies were not congruent with those of the host, indicating that the evolution of the social bee gut microbiota was not driven by strict codiversification but included host switches and independent symbiont gain and losses. Finally, as reported for the honey bee and bumblebee microbiotas, we found substantial genomic divergence among strains of stingless bee gut bacteria, suggesting adaptation to different host species and glycan niches. Our study offers first insights into the genomic diversity of the stingless bee microbiota and highlights the need for broader samplings to understand the evolution of the social bee gut microbiota. IMPORTANCE Stingless bees are the most diverse group of the corbiculate bees and represent important pollinator species throughout the tropics and subtropics. They harbor specialized microbial communities in their gut that are related to those found in honey bees and bumblebees and that are likely important for bee health. Few bacteria have been cultured from the gut of stingless bees, which has prevented characterization of their genomic diversity and functional potential. Here, we established cultures of major members of the gut microbiotas of six stingless bee species and sequenced their genomes. We found that most stingless bee isolates belong to novel bacterial species distantly related to those found in honey bees and bumblebees and encoding similar functional capabilities. Our study offers a new perspective on the evolution of the social bee gut microbiota and presents a basis for characterizing the symbiotic relationships between gut bacteria and stingless bees.https://journals.asm.org/doi/10.1128/mbio.03538-22bacteriadiversificationgenomegut microbiomeinsectsphylogeny
spellingShingle Garance Sarton-Lohéac
Carlos Gustavo Nunes da Silva
Florent Mazel
Gilles Baud
Vincent de Bakker
Sudip Das
Yassine El Chazli
Kirsten Ellegaard
Marc Garcia-Garcera
Natasha Glover
Joanito Liberti
Lorena Nacif Marçal
Aiswarya Prasad
Vincent Somerville
Germán Bonilla-Rosso
Philipp Engel
Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees
mBio
bacteria
diversification
genome
gut microbiome
insects
phylogeny
title Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees
title_full Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees
title_fullStr Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees
title_full_unstemmed Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees
title_short Deep Divergence and Genomic Diversification of Gut Symbionts of Neotropical Stingless Bees
title_sort deep divergence and genomic diversification of gut symbionts of neotropical stingless bees
topic bacteria
diversification
genome
gut microbiome
insects
phylogeny
url https://journals.asm.org/doi/10.1128/mbio.03538-22
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