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Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome

The gut of the European honey bee (Apis mellifera) possesses a relatively simple bacterial community, but little is known about its community of prophages (temperate bacteriophages integrated into the bacterial genome). Although prophages may eventually begin replicating and kill their bacterial hos...

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Autores principales: Bueren, Emma K., Weinheimer, Alaina R., Aylward, Frank O., Hsu, Bryan B., Haak, David C., Belden, Lisa K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259446/
https://www.ncbi.nlm.nih.gov/pubmed/37312882
http://dx.doi.org/10.7717/peerj.15383
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author Bueren, Emma K.
Weinheimer, Alaina R.
Aylward, Frank O.
Hsu, Bryan B.
Haak, David C.
Belden, Lisa K.
author_facet Bueren, Emma K.
Weinheimer, Alaina R.
Aylward, Frank O.
Hsu, Bryan B.
Haak, David C.
Belden, Lisa K.
author_sort Bueren, Emma K.
collection PubMed
description The gut of the European honey bee (Apis mellifera) possesses a relatively simple bacterial community, but little is known about its community of prophages (temperate bacteriophages integrated into the bacterial genome). Although prophages may eventually begin replicating and kill their bacterial hosts, they can also sometimes be beneficial for their hosts by conferring protection from other phage infections or encoding genes in metabolic pathways and for toxins. In this study, we explored prophages in 17 species of core bacteria in the honey bee gut and two honey bee pathogens. Out of the 181 genomes examined, 431 putative prophage regions were predicted. Among core gut bacteria, the number of prophages per genome ranged from zero to seven and prophage composition (the compositional percentage of each bacterial genome attributable to prophages) ranged from 0 to 7%. Snodgrassella alvi and Gilliamella apicola had the highest median prophages per genome (3.0 ± 1.46; 3.0 ± 1.59), as well as the highest prophage composition (2.58% ± 1.4; 3.0% ± 1.59). The pathogen Paenibacillus larvae had a higher median number of prophages (8.0 ± 5.33) and prophage composition (6.40% ± 3.08) than the pathogen Melissococcus plutonius or any of the core bacteria. Prophage populations were highly specific to their bacterial host species, suggesting most prophages were acquired recently relative to the divergence of these bacterial groups. Furthermore, functional annotation of the predicted genes encoded within the prophage regions indicates that some prophages in the honey bee gut encode additional benefits to their bacterial hosts, such as genes in carbohydrate metabolism. Collectively, this survey suggests that prophages within the honey bee gut may contribute to the maintenance and stability of the honey bee gut microbiome and potentially modulate specific members of the bacterial community, particularly S. alvi and G. apicola.
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spelling pubmed-102594462023-06-13 Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome Bueren, Emma K. Weinheimer, Alaina R. Aylward, Frank O. Hsu, Bryan B. Haak, David C. Belden, Lisa K. PeerJ Entomology The gut of the European honey bee (Apis mellifera) possesses a relatively simple bacterial community, but little is known about its community of prophages (temperate bacteriophages integrated into the bacterial genome). Although prophages may eventually begin replicating and kill their bacterial hosts, they can also sometimes be beneficial for their hosts by conferring protection from other phage infections or encoding genes in metabolic pathways and for toxins. In this study, we explored prophages in 17 species of core bacteria in the honey bee gut and two honey bee pathogens. Out of the 181 genomes examined, 431 putative prophage regions were predicted. Among core gut bacteria, the number of prophages per genome ranged from zero to seven and prophage composition (the compositional percentage of each bacterial genome attributable to prophages) ranged from 0 to 7%. Snodgrassella alvi and Gilliamella apicola had the highest median prophages per genome (3.0 ± 1.46; 3.0 ± 1.59), as well as the highest prophage composition (2.58% ± 1.4; 3.0% ± 1.59). The pathogen Paenibacillus larvae had a higher median number of prophages (8.0 ± 5.33) and prophage composition (6.40% ± 3.08) than the pathogen Melissococcus plutonius or any of the core bacteria. Prophage populations were highly specific to their bacterial host species, suggesting most prophages were acquired recently relative to the divergence of these bacterial groups. Furthermore, functional annotation of the predicted genes encoded within the prophage regions indicates that some prophages in the honey bee gut encode additional benefits to their bacterial hosts, such as genes in carbohydrate metabolism. Collectively, this survey suggests that prophages within the honey bee gut may contribute to the maintenance and stability of the honey bee gut microbiome and potentially modulate specific members of the bacterial community, particularly S. alvi and G. apicola. PeerJ Inc. 2023-06-09 /pmc/articles/PMC10259446/ /pubmed/37312882 http://dx.doi.org/10.7717/peerj.15383 Text en ©2023 Bueren et al. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Entomology
Bueren, Emma K.
Weinheimer, Alaina R.
Aylward, Frank O.
Hsu, Bryan B.
Haak, David C.
Belden, Lisa K.
Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome
title Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome
title_full Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome
title_fullStr Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome
title_full_unstemmed Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome
title_short Characterization of prophages in bacterial genomes from the honey bee (Apis mellifera) gut microbiome
title_sort characterization of prophages in bacterial genomes from the honey bee (apis mellifera) gut microbiome
topic Entomology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259446/
https://www.ncbi.nlm.nih.gov/pubmed/37312882
http://dx.doi.org/10.7717/peerj.15383
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