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Higher Variability in Fungi Compared to Bacteria in the Foraging Honey Bee Gut

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Abstract

Along with bacteria, fungi can represent a significant component of animal- and plant-associated microbial communities. However, we have only begun to describe these fungi, much less examine their effects on most animals and plants. Bacteria associated with the honey bee, Apis mellifera, have been well characterized across different regions of the gut. The mid- and hindgut of foraging bees house a deterministic set of core species that affect host health, whereas the crop, or the honey stomach, harbors a more diverse set of bacteria that is highly variable in composition among individual bees. Whether this contrast between the two regions of the gut also applies to fungi remains unclear despite their potential influence on host health. In honey bees caught foraging at four sites across the San Francisco Peninsula of California, we found that fungi were less distinct in species composition between the crop and the mid- and hindgut than bacteria. Unlike bacteria, fungi varied substantially in species composition throughout the honey bee gut, and much of this variation could be predicted by the location where we collected the bees. These observations suggest that fungi may be transient passengers and unimportant as gut symbionts. However, our findings also indicate that honey bees could be vectors of infectious plant diseases as many of the fungi we found in the honey bee gut are recognized as plant pathogens.

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Data Availability

Raw sequence data are openly available in the Sequence Read Archives of the National Center for Biotechnology Information (NCBI), accession number: PRJNA775827. URL: https://www.ncbi.nlm.nih.gov/bioproject/PRJNA775827

Code Availability

Upon acceptance, code will be made available on Dryad Digital Repository.

References

  1. Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol. https://doi.org/10.1128/AEM.07810-11

    Article  Google Scholar 

  2. Zheng H, Steele MI, Leonard SP et al (2018) Honey bees as models for gut microbiota research. Lab Anim (NY) 47:317–325

    Article  Google Scholar 

  3. Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384. https://doi.org/10.1038/nrmicro.2016.43

    Article  CAS  Google Scholar 

  4. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci 109:11002–11007. https://doi.org/10.1073/pnas.1202970109

    Article  Google Scholar 

  5. Moran NA, Hansen AK, Powell JE, Sabree ZL (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE 7:e36393. https://doi.org/10.1371/journal.pone.0036393

    Article  CAS  Google Scholar 

  6. Kešnerová L, Emery O, Troilo M et al (2020) Gut microbiota structure differs between honeybees in winter and summer. ISME J 14:801–814. https://doi.org/10.1038/s41396-019-0568-8

    Article  Google Scholar 

  7. Corby-Harris V, Maes P, Anderson KE (2014) The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE 9:e95056. https://doi.org/10.1371/journal.pone.0095056

    Article  CAS  Google Scholar 

  8. Anderson KE, Sheehan TH, Mott BM et al (2013) Microbial ecology of the hive and oollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS ONE 8:e83125. https://doi.org/10.1371/journal.pone.0083125

    Article  CAS  Google Scholar 

  9. Arredondo D, Castelli L, Porrini MP et al (2018) Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Benef Microbes 9:279–290. https://doi.org/10.3920/BM2017.0075

    Article  CAS  Google Scholar 

  10. Daisley BA, Pitek AP, Chmiel JA et al (2020) Novel probiotic approach to counter Paenibacillus larvae infection in honey bees. ISME J 14:476–491. https://doi.org/10.1038/s41396-019-0541-6

    Article  CAS  Google Scholar 

  11. Stefanini I (2018) Yeast-insect associations: it takes guts. Yeast 35:315–330. https://doi.org/10.1002/yea.3309

    Article  CAS  Google Scholar 

  12. Yun JH, Jung MJ, Kim PS, Bae JW (2018) Social status shapes the bacterial and fungal gut communities of the honey bee. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-19860-7

    Article  CAS  Google Scholar 

  13. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc 18:315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1

    Article  Google Scholar 

  14. Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584

    Article  Google Scholar 

  15. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth0510-335

    Article  CAS  Google Scholar 

  16. Nilsson RH, Larsson KH, Taylor AFS et al (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264. https://doi.org/10.1093/nar/gky1022

    Article  CAS  Google Scholar 

  17. Vannette RL, Fukami T (2017) Dispersal enhances beta diversity in nectar microbes. Ecol Lett 20:901–910. https://doi.org/10.1111/ele.12787

    Article  Google Scholar 

  18. Chazdon RL, Chao A, Colwell RK et al (2011) A novel statistical method for classifying habitat generalists and specialists. Ecology 92:1332–1343. https://doi.org/10.1890/10-1345.1

    Article  Google Scholar 

  19. Ptaszyńska AA, Paleolog J, Borsuk G (2016) Nosema ceranae infection promotes proliferation of yeasts in honey bee intestines. PLoS ONE 11:e0164477. https://doi.org/10.1371/journal.pone.0164477

    Article  CAS  Google Scholar 

  20. Parish JB, Scott ES, Correll R, Hogendoorn K (2019) Survival and probability of transmission of plant pathogenic fungi through the digestive tract of honey bee workers. Apidologie 50:871–880. https://doi.org/10.1007/s13592-019-00697-6

    Article  CAS  Google Scholar 

  21. Alexandrova M, Cimini B, Bazzi C et al (2002) The role of honeybees in spreading Erwinia amylovora. IX International Workshop on Fire Blight 590:55–60

    Google Scholar 

  22. Gasparoto MCG, Lourenço SA, Tanaka FAO et al (2017) Honeybees can spread Colletotrichum acutatum and C. gloeosporioides among citrus plants. Plant Pathol 66:777–782. https://doi.org/10.1111/ppa.12625

    Article  CAS  Google Scholar 

  23. Rucker RR, Thurman WN, Burgett M (2012) Honey bee pollination markets and the internalization of reciprocal benefits. Am J Agric Econ 94:956–977. https://doi.org/10.1093/ajae/aas031

    Article  Google Scholar 

  24. Regan T, Barnett MW, Laetsch DR et al (2018) Characterisation of the British honey bee metagenome. Nat Commun 9:1–13. https://doi.org/10.1038/s41467-018-07426-0

    Article  CAS  Google Scholar 

  25. Foley K, Fazio G, Jensen AB, Hughes WOH (2014) The distribution of Aspergillus spp. opportunistic parasites in hives and their pathogenicity to honey bees. Vet Microbiol 169:203–210. https://doi.org/10.1016/j.vetmic.2013.11.029

    Article  Google Scholar 

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Acknowledgements

We thank Megan Morris for advice on DNA extraction, sequencing, and data analysis. We also thank Callie Chappell, Nick Hendershot, Jesse Miller, Chih-Fu Yeh, and two anonymous reviewers for comments.

Funding

This work was funded by NSF (DEB 1737758). CED was supported by the Stanford Summer Research Program.

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Authors

Contributions

LED, PAS, CED, MLW, and TF designed the study, and LED, PAS, CED, and MLW collected samples. LED and CG analyzed data, and LED wrote the first draft of the manuscript. All authors contributed to editing the manuscript.

Corresponding author

Correspondence to Leslie E. Decker.

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The authors declare no competing interests.

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Decker, L.E., San Juan, P.A., Warren, M.L. et al. Higher Variability in Fungi Compared to Bacteria in the Foraging Honey Bee Gut. Microb Ecol 85, 330–334 (2023). https://doi.org/10.1007/s00248-021-01922-5

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