Honey bee genetics shape the strain-level structure of gut microbiota in social transmission

Abstract 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 struc...

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Autores principales:	Jiaqiang Wu, Haoyu Lang, Xiaohuan Mu, Zijing Zhang, Qinzhi Su, Xiaosong Hu, Hao Zheng
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Apis mellifera Gut microbiota GWAS Bifidobacterium Host specificity Type IV pili Microbial ecology QR100-130
Acceso en línea:	https://doaj.org/article/f18fb949409d458eb4cf0702a2466f92
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spelling	oai:doaj.org-article:f18fb949409d458eb4cf0702a2466f922021-11-21T12:06:39ZHoney bee genetics shape the strain-level structure of gut microbiota in social transmission10.1186/s40168-021-01174-y2049-2618https://doaj.org/article/f18fb949409d458eb4cf0702a2466f922021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01174-yhttps://doaj.org/toc/2049-2618Abstract 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. Video abstractJiaqiang WuHaoyu LangXiaohuan MuZijing ZhangQinzhi SuXiaosong HuHao ZhengBMCarticleApis melliferaGut microbiotaGWASBifidobacteriumHost specificityType IV piliMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-19 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Apis mellifera Gut microbiota GWAS Bifidobacterium Host specificity Type IV pili Microbial ecology QR100-130
spellingShingle	Apis mellifera Gut microbiota GWAS Bifidobacterium Host specificity Type IV pili Microbial ecology QR100-130 Jiaqiang Wu Haoyu Lang Xiaohuan Mu Zijing Zhang Qinzhi Su Xiaosong Hu Hao Zheng Honey bee genetics shape the strain-level structure of gut microbiota in social transmission
description	Abstract 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. Video abstract
format	article
author	Jiaqiang Wu Haoyu Lang Xiaohuan Mu Zijing Zhang Qinzhi Su Xiaosong Hu Hao Zheng
author_facet	Jiaqiang Wu Haoyu Lang Xiaohuan Mu Zijing Zhang Qinzhi Su Xiaosong Hu Hao Zheng
author_sort	Jiaqiang Wu
title	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_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_sort	honey bee genetics shape the strain-level structure of gut microbiota in social transmission
publisher	BMC
publishDate	2021
url	https://doaj.org/article/f18fb949409d458eb4cf0702a2466f92
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Honey bee genetics shape the strain-level structure of gut microbiota in social transmission

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