The gut microbiome in deformed wing virus (DWV)-uninfected and -infected Apis cerana honeybees suggests the role of gut microbiota in combating viral infections
Author affiliations
DOI:
https://doi.org/10.15625/2615-9023/20923Abstract
Honeybees harbor a distinct core microbiota that plays a crucial role in stress tolerance and disease resistance. However, infections can significantly alter the composition and diversity of their gut microbiota, impacting overall bee health. This study investigates the effects of Deformed Wing Virus (DWV) infection on the gut microbiota of Apis cerana honeybee. The samples were collected from six colonies in Hanoi, Vietnam, and analyzed using high-throughput sequencing of the 16S rRNA gene. Our results show that while the overall diversity of gut microbiota in DWV-infected and uninfected bees did not significantly differ, notable changes were observed in the relative abundances of specific bacterial taxa. In DWV-infected bees, the relative abundance of Proteobacteria significantly decreased, whereas Firmicutes increased compared to uninfected bees. At the genus level, a significant decrease in Gilliamella and an increase in Lactobacillus were observed in infected bees. Functional gene predictions indicated that pathways related to carbohydrate, fatty acid, and lipid metabolism, as well as the biosynthesis of cofactors, vitamins, and amino acids, were upregulated in DWV-infected bees. These findings highlight the impact of DWV infection on the gut microbiota of A. cerana and suggest potential avenues for using probiotics to restore gut microbial balance and improve honeybee health. This research provides a foundation for developing strategies to enhance the resilience of honeybee colonies against viral infections.
Downloads
Metrics
References
Anderson K. E., Sheehan T. H., Mott B. M., Maes P., Snyder L., Schwan M. R., . . . Corby-Harris V., 2013. Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One, 8(12): e83125.
Audisio M. C., 2017. Gram-positive bacteria with probiotic potential for the Apis mellifera L. honey bee: the experience in the northwest of Argentina. Probiotics and Antimicrobial Proteins, 9(1): 22−31.
Baffoni L., Gaggìa F., Alberoni D., Cabbri R., Nanetti A., Biavati B., & Di Gioia D., 2016. Effect of dietary supplementation of Bifidobacterium and Lactobacillus strains in Apis mellifera L. against Nosema ceranae. Beneficial Microbes, 7(1): 45−51.
Budge G. E., Pietravalle S., Brown M., Laurenson L., Jones B., Tomkies V., & Delaplane K. S., 2015. Pathogens as predictors of honey bee colony strength in England and Wales. PLoS One, 10(7): e0133228.
Cai X. T., Li H., Borch Jensen M., Maksoud E., Borneo J., Liang Y., . . . Jasper H., 2021. Gut cytokines modulate olfaction through metabolic reprogramming of glia. Nature, 596(7870): 97−102.
Callahan B. J., McMurdie P. J., Rosen M. J., Han A. W., Johnson A. J. A., & Holmes S. P., 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature methods, 13(7): 581−583.
Cox-Foster D. L., Conlan S., Holmes E. C., Palacios G., Evans J. D., Moran N. A., . . . Geiser D. M., 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318(5848): 283−287.
Daisley B. A., Chmiel J. A., Pitek A. P., Thompson G. J., & Reid G., 2020. Missing microbes in bees: how systematic depletion of key symbionts erodes immunity. Trends in Microbiology, 28(12): 1010−1021.
Deitch E. A., Xu D., Qi L., & Berg R. D., 1991. Bacterial translocation from the gut impairs systemic immunity. Surgery, 109(3 Pt 1): 269−276.
Dosch C., Manigk A., Streicher T., Tehel A., Paxton R. J., & Tragust S., 2021. The gut microbiota can provide viral tolerance in the honey bee. Microorganisms, 9(4): 871.
Douglas G. M., Maffei V. J., Zaneveld J. R., Yurgel S. N., Brown J. R., Taylor C. M., . . . Langille M. G., 2020. PICRUSt2 for prediction of metagenome functions. Nature biotechnology, 38(6): 685−688.
Duong B. T. T., Lien N. T. K., Thu H. T., Hoa N. T., Lanh P. T., Yun B.-R., . . . Van Quyen D., 2020. Investigation of the gut microbiome of Apis cerana honeybees from Vietnam. Biotechnology Letters, 42(11): 2309−2317.
Eichler S., & Schaub G., 2002. Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Experimental parasitology, 100(1): 17−27.
Ellegaard K. M., & Engel P., 2019. Genomic diversity landscape of the honey bee gut microbiota. Nature communications, 10(1): 446.
Endo A., & Salminen S., 2013. Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Systematic and Applied Microbiology, 36(6): 444−448.
Engel P., Martinson V. G., & Moran N. A., 2012. Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences, 109(27): 11002−11007.
Engel P., & Moran N. A., 2013. The gut microbiota of insects–diversity in structure and function. FEMS microbiology reviews, 37(5): 699−735.
Engel P., Stepanauskas R., & Moran N. A., 2014. Hidden diversity in honey bee gut symbionts detected by single-cell genomics. PLoS genetics, 10(9): e1004596.
Genersch E., & Aubert M., 2010. Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Veterinary research, 41(6).
Hubert J., Bicianova M., Ledvinka O., Kamler M., Lester P. J., Nesvorna M., . . . Erban T., 2017. Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microbial ecology, 73: 685−698.
Kešnerová L., Moritz R., & Engel P., 2016. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. International journal of systematic and evolutionary microbiology, 66(1): 414−421.
Koch H., & Schmid-Hempel P., 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences, 108(48): 19288−19292.
Kwong W. K., & Moran N. A., 2016. Gut microbial communities of social bees. Nature Reviews Microbiology, 14(6): 374−384.
Lanh P. T., Duong B. T., Thu H. T., Hoa N. T., & Van Quyen D., 2024. Comprehensive analysis of the microbiome in Apis cerana honey highlights honey as a potential source for the isolation of beneficial bacterial strains. PeerJ, 12: e17157.
Li J., Heerman M. C., Evans J. D., Rose R., Li W., Rodríguez-García C., . . . Li Z., 2019. Pollen reverses decreased lifespan, altered nutritional metabolism and suppressed immunity in honey bees (Apis mellifera) treated with antibiotics. Journal of Experimental Biology, 222(7): jeb202077.
Ma W., Zheng X., Li L., Shen J., Li W., & Gao Y., 2020. Changes in the gut microbiota of honey bees associated with jujube flower disease. Ecotoxicology and Environmental Safety, 198: 110616.
Panjad P., Yongsawas R., Sinpoo C., Pakwan C., Subta P., Krongdang S., Disayathanoowat T., 2021. Impact of Nosema disease and American foulbrood on gut bacterial communities of honeybees Apis mellifera. Insects, 12(6): 525.
Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., . . . Glöckner F. O., 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic acids research, 41(D1): D590-D596.
Raymann K., & Moran N. A., 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Current opinion in insect science, 26: 97−104.
Raymann K., Shaffer Z., & Moran N. A., 2017. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS biology, 15(3): e2001861.
Saraiva M. A., Zemolin A. P. P., Franco J. L., Boldo J. T., Stefenon V. M., Triplett E. W., Roesch L. F. W., 2015. Relationship between honeybee nutrition and their microbial communities. Antonie Van Leeuwenhoek, 107: 921−933.
Silva M. S., Rabadzhiev Y., Eller M. R., Iliev I., Ivanova I., & Santana W. C., 2017. Microorganisms in honey. Honey analysis, 500: 233−257.
Spivak M., & Reuter G. S., 2001. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie, 32(6): 555−565.
Tantillo G., Bottaro M., Di Pinto A., Martella V., Di Pinto P., & Terio V., 2015. Virus infections of honeybees Apis mellifera. Italian journal of food safety, 4(3).
Vásquez A., Forsgren E., Fries I., Paxton R. J., Flaberg E., Szekely L., & Olofsson T. C., 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS one, 7(3): e33188.
Wu M., Sugimura Y., Taylor D., & Yoshiyama M., 2013. Honeybee gastrointestinal bacteria for novel and sustainable disease control strategies. Journal of Developments in Sustainable Agriculture, 8(2): 85−90.
Yun B.-R., Truong A.-T., Choi Y. S., Lee M. Y., Kim B. Y., Seo M., . . . Cho Y. S., 2022. Comparison of the gut microbiome of sacbrood virus-resistant and-susceptible Apis cerana from South Korea. Scientific Reports, 12(1): 10010.
Zhang Z., Mu X., Shi Y., & Zheng H., 2022. Distinct roles of honeybee gut bacteria on host metabolism and neurological processes. Microbiology Spectrum, 10(2): e02438-02421.
Zheng H., Perreau J., Powell J. E., Han B., Zhang Z., Kwong W. K., Moran N. A., 2019. Division of labor in honey bee gut microbiota for plant polysaccharide digestion. Proceedings of the National Academy of Sciences, 116(51): 25909−25916.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Dong Van Quyen, Pham Thi Lanh
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.