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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Main Authors: Qinzhi Su, Qinglin Wang, Xiaohuan Mu, Hao Chen, Yujie Meng, Xue Zhang, Li Zheng, Xiaosong Hu, Yifan Zhai, Hao Zheng
Format: Article
Language:English
Published: BMC 2021-11-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-021-01163-1
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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
collection DOAJ
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
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spelling doaj.art-9234504eb30847f5a920bcd5c8d2244d2022-12-21T23:00:29ZengBMCMicrobiome2049-26182021-11-019111410.1186/s40168-021-01163-1Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebeeQinzhi Su0Qinglin Wang1Xiaohuan Mu2Hao Chen3Yujie Meng4Xue Zhang5Li Zheng6Xiaosong Hu7Yifan Zhai8Hao Zheng9College of Food Science and Nutritional Engineering, China Agricultural UniversityCollege of Food Science and Nutritional Engineering, China Agricultural UniversityCollege of Food Science and Nutritional Engineering, China Agricultural UniversityShandong Institute of Plant Protection, Shandong Academy of Agricultural SciencesCollege of Food Science and Nutritional Engineering, China Agricultural UniversityDepartment of Entomology, College of Plant Protection, China Agricultural UniversityShandong Institute of Plant Protection, Shandong Academy of Agricultural SciencesCollege of Food Science and Nutritional Engineering, China Agricultural UniversityShandong Institute of Plant Protection, Shandong Academy of Agricultural SciencesCollege of Food Science and Nutritional Engineering, China Agricultural UniversityAbstract 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 Abstracthttps://doi.org/10.1186/s40168-021-01163-1Bombus terrestrisApis melliferaApis ceranaGut microbiotaStrain diversityVertical transmission
spellingShingle 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
Microbiome
Bombus terrestris
Apis mellifera
Apis cerana
Gut microbiota
Strain diversity
Vertical transmission
title 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_short 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
topic Bombus terrestris
Apis mellifera
Apis cerana
Gut microbiota
Strain diversity
Vertical transmission
url https://doi.org/10.1186/s40168-021-01163-1
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