Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages
ABSTRACTIn eusocial insects, the health of the queens—the colony founders and sole reproductive females—is a primary determinant for colony success. Queen failure in the honey bee Apis mellifera, for example, is a major concern of beekeepers who annually suffer colony losses, necessitating a greater...
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2024-02-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01182-23 |
| _version_ | 1827346461860298752 |
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| author | Lílian Caesar Danny W. Rice Alison McAfee Robyn Underwood Carrie Ganote David R. Tarpy Leonard J. Foster Irene L. G. Newton |
| author_facet | Lílian Caesar Danny W. Rice Alison McAfee Robyn Underwood Carrie Ganote David R. Tarpy Leonard J. Foster Irene L. G. Newton |
| author_sort | Lílian Caesar |
| collection | DOAJ |
| description | ABSTRACTIn eusocial insects, the health of the queens—the colony founders and sole reproductive females—is a primary determinant for colony success. Queen failure in the honey bee Apis mellifera, for example, is a major concern of beekeepers who annually suffer colony losses, necessitating a greater knowledge of queen health. Several studies on the microbiome of honey bees have characterized its diversity and shown its importance for the health of worker bees, the female non-reproductive caste. However, the microbiome of workers differs from that of queens, which, in comparison, is still poorly studied. Thus, direct investigations of the queen microbiome are required to understand colony-level microbiome assembly, functional roles, and evolution. Here, we used metagenomics to comprehensively characterize the honey bee queen microbiome. Comparing samples from different geographic locations and breeder sources, we show that the microbiome of queens is mostly shaped by the environment experienced since early life and is predicted to play roles in the breakdown of the diet and protection from pathogens and xenobiotics. We also reveal that the microbiome of queens comprises only four candidate core bacterial species, Apilactobacillus kunkeei, Lactobacillus apis, Bombella apis, and Commensalibacter sp. Interestingly, in addition to bacteria, we show that bacteriophages infect the queen microbiome, for which Lactobacillaceae are predicted to be the main reservoirs. Together, our results provide the basis to understand the honey bee colony microbiome assemblage, can guide improvements in queen-rearing processes, and highlight the importance of considering bacteriophages for queen microbiome health and microbiome homeostasis in eusocial insects.IMPORTANCEThe queen caste plays a central role in colony success in eusocial insects, as queens lay eggs and regulate colony behavior and development. Queen failure can cause colonies to collapse, which is one of the major concerns of beekeepers. Thus, understanding the biology behind the queen’s health is a pressing issue. Previous studies have shown that the bee microbiome plays an important role in worker bee health, but little is known about the queen microbiome and its function in vivo. Here, we characterized the queen microbiome, identifying for the first time the present species and their putative functions. We show that the queen microbiome has predicted nutritional and protective roles in queen association and comprises only four consistently present bacterial species. Additionally, we bring to attention the spread of phages in the queen microbiome, which increased in abundance in failing queens and may impact the fate of the colony. |
| first_indexed | 2024-03-07T23:31:32Z |
| format | Article |
| id | doaj.art-643172ffc82e4d96bcf8f2ea114b45ad |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-07T23:31:32Z |
| publishDate | 2024-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-643172ffc82e4d96bcf8f2ea114b45ad2024-02-20T14:00:48ZengAmerican Society for MicrobiologymSystems2379-50772024-02-019210.1128/msystems.01182-23Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phagesLílian Caesar0Danny W. Rice1Alison McAfee2Robyn Underwood3Carrie Ganote4David R. Tarpy5Leonard J. Foster6Irene L. G. Newton7Department of Biology, Indiana University, Bloomington, Indiana, USADepartment of Biology, Indiana University, Bloomington, Indiana, USADepartment of Biochemistry and Molecular Biology, Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia, CanadaDepartment of Entomology, Pennsylvania State University, University Park, State College, Pennsylvania, USALuddy School of Informatics, Indiana University, Bloomington, Indiana, USADepartment of Applied Ecology, North Carolina State University, Raleigh, North Carolina, USADepartment of Biochemistry and Molecular Biology, Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia, CanadaDepartment of Biology, Indiana University, Bloomington, Indiana, USAABSTRACTIn eusocial insects, the health of the queens—the colony founders and sole reproductive females—is a primary determinant for colony success. Queen failure in the honey bee Apis mellifera, for example, is a major concern of beekeepers who annually suffer colony losses, necessitating a greater knowledge of queen health. Several studies on the microbiome of honey bees have characterized its diversity and shown its importance for the health of worker bees, the female non-reproductive caste. However, the microbiome of workers differs from that of queens, which, in comparison, is still poorly studied. Thus, direct investigations of the queen microbiome are required to understand colony-level microbiome assembly, functional roles, and evolution. Here, we used metagenomics to comprehensively characterize the honey bee queen microbiome. Comparing samples from different geographic locations and breeder sources, we show that the microbiome of queens is mostly shaped by the environment experienced since early life and is predicted to play roles in the breakdown of the diet and protection from pathogens and xenobiotics. We also reveal that the microbiome of queens comprises only four candidate core bacterial species, Apilactobacillus kunkeei, Lactobacillus apis, Bombella apis, and Commensalibacter sp. Interestingly, in addition to bacteria, we show that bacteriophages infect the queen microbiome, for which Lactobacillaceae are predicted to be the main reservoirs. Together, our results provide the basis to understand the honey bee colony microbiome assemblage, can guide improvements in queen-rearing processes, and highlight the importance of considering bacteriophages for queen microbiome health and microbiome homeostasis in eusocial insects.IMPORTANCEThe queen caste plays a central role in colony success in eusocial insects, as queens lay eggs and regulate colony behavior and development. Queen failure can cause colonies to collapse, which is one of the major concerns of beekeepers. Thus, understanding the biology behind the queen’s health is a pressing issue. Previous studies have shown that the bee microbiome plays an important role in worker bee health, but little is known about the queen microbiome and its function in vivo. Here, we characterized the queen microbiome, identifying for the first time the present species and their putative functions. We show that the queen microbiome has predicted nutritional and protective roles in queen association and comprises only four consistently present bacterial species. Additionally, we bring to attention the spread of phages in the queen microbiome, which increased in abundance in failing queens and may impact the fate of the colony.https://journals.asm.org/doi/10.1128/msystems.01182-23symbiosisbacteriophageeusocial insectgenetic backgroundApis mellifera |
| spellingShingle | Lílian Caesar Danny W. Rice Alison McAfee Robyn Underwood Carrie Ganote David R. Tarpy Leonard J. Foster Irene L. G. Newton Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages mSystems symbiosis bacteriophage eusocial insect genetic background Apis mellifera |
| title | Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages |
| title_full | Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages |
| title_fullStr | Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages |
| title_full_unstemmed | Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages |
| title_short | Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages |
| title_sort | metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and caudoviricetes phages |
| topic | symbiosis bacteriophage eusocial insect genetic background Apis mellifera |
| url | https://journals.asm.org/doi/10.1128/msystems.01182-23 |
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