Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee

Abstract Background Microbial acquisition and development of the gut microbiota impact the establishment of a healthy host-microbes symbiosis. Compared with other animals, the eusocial bumblebees and honeybees possess a simple, recurring, and similar set of gut microbiota. However, all bee gut phylo...

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Autores principales:	Qinzhi Su, Qinglin Wang, Xiaohuan Mu, Hao Chen, Yujie Meng, Xue Zhang, Li Zheng, Xiaosong Hu, Yifan Zhai, Hao Zheng
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Bombus terrestris Apis mellifera Apis cerana Gut microbiota Strain diversity Vertical transmission Microbial ecology QR100-130
Acceso en línea:	https://doaj.org/article/9234504eb30847f5a920bcd5c8d2244d
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spelling	oai:doaj.org-article:9234504eb30847f5a920bcd5c8d2244d2021-11-07T12:12:22ZStrain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee10.1186/s40168-021-01163-12049-2618https://doaj.org/article/9234504eb30847f5a920bcd5c8d2244d2021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01163-1https://doaj.org/toc/2049-2618Abstract Background Microbial acquisition and development of the gut microbiota impact the establishment of a healthy host-microbes symbiosis. Compared with other animals, the eusocial bumblebees and honeybees possess a simple, recurring, and similar set of gut microbiota. However, all bee gut phylotypes have high strain-level diversity. Gut communities of different bee species are composed of host-specific groups of strains. The variable genomic regions among strains of the same species often confer critical functional differences, such as carbon source utilization, essential for the natural selection of specific strains. The annual bumblebee colony founded by solitary queens enables tracking the transmission routes of gut bacteria during development stages. Results Here, we first showed the changes in the microbiome of individual bumblebees across their holometabolous life cycle. Some core gut bacteria persist throughout different stages of development. Gut microbiota of newly emerged workers always resembles those of their queens, suggesting a vertical transmission of strains from queens to the newborn workers. We then follow the dynamic changes in the gut community by comparing strain-level metagenomic profiles of queen-worker pairs longitudinally collected across different stages of the nest development. Species composition of both queen and worker shifts with the colony’s growth, and the queen-to-worker vertical inheritance of specific strains was identified. Finally, comparative metagenome analysis showed clear host-specificity for microbes across different bee hosts. Species from honeybees often possess a higher level of strain variation, and they also exhibited more complex gene repertoires linked to polysaccharide digestion. Our results demonstrate bacterial transmission events in bumblebee, highlighting the role of social interactions in driving the microbiota composition. Conclusions By the community-wide metagenomic analysis based on the custom genomic database of bee gut bacteria, we reveal strain transmission events at high resolution and the dynamic changes in community structure along with the colony development. The social annual life cycle of bumblebees is key for the acquisition and development of the gut microbiota. Further studies using the bumblebee model will advance our understanding of the microbiome transmission and the underlying mechanisms, such as strain competition and niche selection. Video AbstractQinzhi SuQinglin WangXiaohuan MuHao ChenYujie MengXue ZhangLi ZhengXiaosong HuYifan ZhaiHao ZhengBMCarticleBombus terrestrisApis melliferaApis ceranaGut microbiotaStrain diversityVertical transmissionMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-14 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bombus terrestris Apis mellifera Apis cerana Gut microbiota Strain diversity Vertical transmission Microbial ecology QR100-130
spellingShingle	Bombus terrestris Apis mellifera Apis cerana Gut microbiota Strain diversity Vertical transmission Microbial ecology QR100-130 Qinzhi Su Qinglin Wang Xiaohuan Mu Hao Chen Yujie Meng Xue Zhang Li Zheng Xiaosong Hu Yifan Zhai Hao Zheng Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
description	Abstract Background Microbial acquisition and development of the gut microbiota impact the establishment of a healthy host-microbes symbiosis. Compared with other animals, the eusocial bumblebees and honeybees possess a simple, recurring, and similar set of gut microbiota. However, all bee gut phylotypes have high strain-level diversity. Gut communities of different bee species are composed of host-specific groups of strains. The variable genomic regions among strains of the same species often confer critical functional differences, such as carbon source utilization, essential for the natural selection of specific strains. The annual bumblebee colony founded by solitary queens enables tracking the transmission routes of gut bacteria during development stages. Results Here, we first showed the changes in the microbiome of individual bumblebees across their holometabolous life cycle. Some core gut bacteria persist throughout different stages of development. Gut microbiota of newly emerged workers always resembles those of their queens, suggesting a vertical transmission of strains from queens to the newborn workers. We then follow the dynamic changes in the gut community by comparing strain-level metagenomic profiles of queen-worker pairs longitudinally collected across different stages of the nest development. Species composition of both queen and worker shifts with the colony’s growth, and the queen-to-worker vertical inheritance of specific strains was identified. Finally, comparative metagenome analysis showed clear host-specificity for microbes across different bee hosts. Species from honeybees often possess a higher level of strain variation, and they also exhibited more complex gene repertoires linked to polysaccharide digestion. Our results demonstrate bacterial transmission events in bumblebee, highlighting the role of social interactions in driving the microbiota composition. Conclusions By the community-wide metagenomic analysis based on the custom genomic database of bee gut bacteria, we reveal strain transmission events at high resolution and the dynamic changes in community structure along with the colony development. The social annual life cycle of bumblebees is key for the acquisition and development of the gut microbiota. Further studies using the bumblebee model will advance our understanding of the microbiome transmission and the underlying mechanisms, such as strain competition and niche selection. Video Abstract
format	article
author	Qinzhi Su Qinglin Wang Xiaohuan Mu Hao Chen Yujie Meng Xue Zhang Li Zheng Xiaosong Hu Yifan Zhai Hao Zheng
author_facet	Qinzhi Su Qinglin Wang Xiaohuan Mu Hao Chen Yujie Meng Xue Zhang Li Zheng Xiaosong Hu Yifan Zhai Hao Zheng
author_sort	Qinzhi Su
title	Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
title_short	Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
title_full	Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
title_fullStr	Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
title_full_unstemmed	Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
title_sort	strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee
publisher	BMC
publishDate	2021
url	https://doaj.org/article/9234504eb30847f5a920bcd5c8d2244d
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Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee

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