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Honey bee genetics shape the strain-level structure of gut microbiota in social transmission
BACKGROUND: Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8597283/ https://www.ncbi.nlm.nih.gov/pubmed/34784973 http://dx.doi.org/10.1186/s40168-021-01174-y |
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author | Wu, Jiaqiang Lang, Haoyu Mu, Xiaohuan Zhang, Zijing Su, Qinzhi Hu, Xiaosong Zheng, Hao |
author_facet | Wu, Jiaqiang Lang, Haoyu Mu, Xiaohuan Zhang, Zijing Su, Qinzhi Hu, Xiaosong Zheng, Hao |
author_sort | Wu, Jiaqiang |
collection | PubMed |
description | BACKGROUND: Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics. RESULTS: We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population” levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain. CONCLUSIONS: Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01174-y. |
format | Online Article Text |
id | pubmed-8597283 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-85972832021-11-17 Honey bee genetics shape the strain-level structure of gut microbiota in social transmission Wu, Jiaqiang Lang, Haoyu Mu, Xiaohuan Zhang, Zijing Su, Qinzhi Hu, Xiaosong Zheng, Hao Microbiome Research BACKGROUND: Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics. RESULTS: We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population” levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain. CONCLUSIONS: Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01174-y. BioMed Central 2021-11-17 /pmc/articles/PMC8597283/ /pubmed/34784973 http://dx.doi.org/10.1186/s40168-021-01174-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Wu, Jiaqiang Lang, Haoyu Mu, Xiaohuan Zhang, Zijing Su, Qinzhi Hu, Xiaosong Zheng, Hao Honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
title | Honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
title_full | Honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
title_fullStr | Honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
title_full_unstemmed | Honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
title_short | Honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
title_sort | honey bee genetics shape the strain-level structure of gut microbiota in social transmission |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8597283/ https://www.ncbi.nlm.nih.gov/pubmed/34784973 http://dx.doi.org/10.1186/s40168-021-01174-y |
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