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

Emma K Bueren; Alaina R Weinheimer; Frank O Aylward; Bryan B Hsu; David C Haak; Lisa K Belden

doi:10.7717/peerj.15383

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

PeerJ. 2023 Jun 9:11:e15383. doi: 10.7717/peerj.15383. eCollection 2023.

Authors

Emma K Bueren¹, Alaina R Weinheimer¹, Frank O Aylward¹, Bryan B Hsu¹, David C Haak², Lisa K Belden¹

Affiliations

¹ Department of Biological Sciences, Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA, United States of America.
² School of Plant and Environmental Sciences, Virginia Polytechnic Institute and State University (Virginia Tech), Blacksburg, VA, United States of America.

Abstract

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.

Keywords: Apis mellifera; Auxillary metabolic genes; Bacteria; Bacteriophage; Honey bee; Lysogen; Phage; Prophage; Symbiosis; Virus.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Bacteriophages*
Bees
Gastrointestinal Microbiome* / genetics
Genome, Bacterial / genetics
Host Specificity
Prophages / genetics

Grants and funding

This research was supported by the National Science Foundation (MCB-1817736). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.