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Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record

Year 2023, Volume: 13 Issue: 1, 592 - 599, 01.03.2023
https://doi.org/10.21597/jist.1204926

Abstract

Gut microbial communities of the honeybee, Apis mellifera L. have vital functions in food digestion, providing essential nutrients, improving immune system against pathogens, and detoxifying harmful molecules. The objective of this study was to characterize the core gut bacterial community of newly emerged A. mellifera queens and workers from southeastern Turkey. A total of newly emerged 15 queens and 30 workers were collected from the same apiary. The alimentary tract of collected samples was dissected under sterile conditions. Culture based isolation was performed from the digestive tract of the collected samples to obtain a pure microbe culture. The chemical, morphological and molecular description of each bacteria were accurately done via employment of pure culture. Five bacterial isolates were successfully isolated from the A. mellifera alimentary tract and purified. Molecular and biochemical identification showed that the isolates were Bacillus pumilus, Bacillus subtilis, Bacillus cereus (Firmicutes: Bacillaceae) (MZ540443, MZ540444, MZ540445), Staphylococcus haemolyticus (Firmicutes: Staphylococcaceae) (MZ540447), and Paenibacillus glucanolyticus (Firmicutes: Paenibacillaceae) (MZ540446). This study is the first to report the presence of P. glucanolyticus in gut bacterial community of A. mellifera.

Supporting Institution

This study was funded by Şırnak University, Research Foundation (Project no: BAP 2019 FNAD 13.02.01).

Project Number

BAP 2019 FNAD 13.02.01

Thanks

I extend my special gratitude to my colleague Mr Metin ERTAŞ (Hakkari University) for his invaluable advises during laboratory studies.

References

  • Alexander, B., Priest, F.G. (1989). Bacillus glucanolyticus, a new species that degrades a variety of β-glucans. International Journal of Systematic and Evolutionary Microbiology, 39: 112-15.
  • Al-Ghamdi, A., Khan, K.A., Ansari, M.J., Almasaudi, S.B., Al-Kahtani, S. (2018). Effect of gut bacterial isolates from Apis mellifera jemenitica on Paenibacillus larvae infected bee larvae. Saudi journal of biological sciences, 25: 383-87.
  • Anjum, S.I., Shah, A.H., Aurongzeb, M., Kori, J., Azim, M.K., Ansari, M.J., Bin, L. (2018). Characterization of gut bacterial flora of Apis mellifera from north-west Pakistan. Saudi journal of biological sciences, 25: 388-92.
  • Cano, R.J., Borucki, M.K., Higby-Schweitzer, M., Poinar, H.N., Poinar Jr, G.O, Pollard KJ, (1994). Bacillus DNA in fossil bees: an ancient symbiosis? Applied and Environmental Microbiology, 60: 2164-67.
  • Chouaia, B., Goda, N., Mazza, G., Alali, S., Florian, F., Gionechetti, F., ... & Montagna, M. (2019). Developmental stages and gut microenvironments influence gut microbiota dynamics in the invasive beetle Popillia japonica Newman (Coleoptera: Scarabaeidae). Environmental microbiology, 21(11), 4343-4359.
  • Corby-Harris, V., Maes, P., Anderson, K.E., (2014). The bacterial communities associated with honey bee (Apis mellifera) foragers. PloS one, 9: e95056.
  • Dal Bello, F., Walter, J., Hertel, C., Hammes, W.P. (2001). In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Systematic and applied microbiology, 24: 232-37
  • Dillon, R.J., Dillon, V., (2004). The gut bacteria of insects: nonpathogenic interactions. Annual Reviews in Entomology, 49: 71-92.
  • Dong, Z.X., Li, H.Y., Chen, Y.F., Wang, F., Deng, X.Y., Lin, L.B., Zhang, Q.L., Li, J.L., Guo, J., (2020). Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiological research, 231: 126370.
  • Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstädter, J., Hurst, G.D. (2008). The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC biology, 6: 1-12.
  • Ellegaard, K.M., Engel, P. (2019). Genomic diversity landscape of the honey bee gut microbiota. Nature communications, 10: 1-13.
  • Ellegaard, K.M., Suenami, S., Miyazaki, R., Engel, P. (2020). Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species. Current biology, 30: 2520-31. e7.
  • Engel, P., Moran, N.A. (2013). The gut microbiota of insects–diversity in structure and function. FEMS microbiology reviews, 37: 699-735.
  • Esawy, M.A., Amer, H., Gamal-Eldeen, A.M., El Enshasy, H.A., Helmy, W.A., Abo-Zeid, M.A., Malek, R., Ahmed, E.F., Awad, G.E. (2013). Scaling up, characterization of levan and its inhibitory role in carcinogenesis initiation stage. Carbohydrate polymers, 95: 578-87
  • Evans, J.D., Armstrong, T.N. (2006). Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC ecology, 6: 1-9.
  • Ganeshprasad, D.N., Lone, J.K., Jani, K., Shouche, Y.S., Khan, K.A., Sayed, S., ... & Sneharani, A. H. (2022). Gut Bacterial Flora of Open Nested Honeybee, Apis florea. Frontiers in Ecology and Evolution, 10.
  • Garrity, G.M., Brenner, D.J., Krieg, N.R., Staley, J.R., & Manual, B.S. (2005). Systematic bacteriology. The Proteobacteria, Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria, Bergey’s Manual Trust, Department of Microbiology and Molecular Genetics, 2.
  • Gebhardt, K., Schimana, J., Müller, J., Fiedler, H.P., Kallenborn, H.G., Holzenkämpfer, M., Krastel, P., Zeeck, A., Vater, J., Höltzel, A., (2002). Screening for biologically active metabolites with endosymbiotic bacilli isolated from arthropods. FEMS Microbiology Letters, 217: 199-205
  • Gilliam, M., (1997). Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiology Letters, 155: 1-10
  • Gomaa, O.M., Momtaz, O.A., City, N., (2007). 16S rRNA characterization of a Bacillus isolate and its tolerance profile after subsequent subculturing. Arab J Biotech, 10: 107-16.
  • Grady, E.N., MacDonald, J., Liu, L., Richman, A., Yuan, Z.C. (2016). Current knowledge and perspectives of Paenibacillus: a review. Microbial cell factories, 15: 1-18.
  • Hamdy, A.A., Elattal, N.A., Amin, M.A., Ali, A.E., Mansour, N.M., Awad, G.E., Awad, H.M., Esawy, M.A. (2017). Possible correlation between levansucrase production and probiotic activity of Bacillus sp. isolated from honey and honey bee. World Journal of Microbiology and Biotechnology, 33: 1-10.
  • Heslop-Harrison, J. (1968). Pollen wall development: the succession of events in the growth of intricately patterned pollen walls is described and discussed. Science, 161: 230-37.
  • Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A., Werren, J.H. (2008). How many species are infected with Wolbachia?–a statistical analysis of current data. FEMS Microbiology Letters, pp. 215-20.
  • Jones, J.C., Fruciano, C., Hildebrand, F., Al Toufalilia, H., Balfour, N.J., Bork, P., Engel, P., Ratnieks F.L., Hughes, W.O. (2018). Gut microbiota composition is associated with environmental landscape in honey bees. Ecology and evolution, 8: 441-51.
  • Kanzawa, Y., Harada, A., Takeuchi, M., Yokota, A., Harada, T., (1995). Bacillus curdlanolyticus sp. nov. and Bacillus kobensis sp. nov., which hydrolyze resistant curdlan. International Journal of Systematic and Evolutionary Microbiology, 45: 515-21.
  • Kapheim, K.M., Rao, V.D., Yeoman, C.J., Wilson, B.A., White, B.A., Goldenfeld, N., Robinson, G.E. (2015). Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PloS one, 10: e0123911.
  • Khan, K.A., Al-Ghamdi, A.A., Ghramh, H.A., Ansari, M.J., Ali, H., Alamri, S.A., Al-Kahtani, S.N., Adgaba, N., Qasim, M., Hafeez, M. (2020). Structural diversity and functional variability of gut microbial communities associated with honey bees. Microbial pathogenesis, 138: 103793.
  • Khan, K.A., Ansari, M.J., Al-Ghamdi, A., Nuru, A., Harakeh, S., Iqbal, J. (2017). Investigation of gut microbial communities associated with indigenous honey bee (Apis mellifera jemenitica) from two different eco-regions of Saudi Arabia. Saudi journal of biological sciences, 24: 1061-68.
  • Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T., (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the royal society B: biological sciences, 274: 303-13.
  • Kumar, S., Stecher, G., Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular biology and evolution, 33: 1870-74.
  • Ludvigsen, J., Porcellato, D., L'Abée‐Lund, T.M., Amdam, G.V., Rudi, K. (2017). Geographical widespread honeybee‐gut symbiont subgroups show locally distinct antibiotic‐resistant patterns. Molecular ecology, 26: 6590-607.
  • Ludvigsen, J., Rangberg, A., Avershina, E., Sekelja, M., Kreibich, C., Amdam, G., Rudi, K. (2015). Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season. Microbes and environments: ME15019.
Year 2023, Volume: 13 Issue: 1, 592 - 599, 01.03.2023
https://doi.org/10.21597/jist.1204926

Abstract

Project Number

BAP 2019 FNAD 13.02.01

References

  • Alexander, B., Priest, F.G. (1989). Bacillus glucanolyticus, a new species that degrades a variety of β-glucans. International Journal of Systematic and Evolutionary Microbiology, 39: 112-15.
  • Al-Ghamdi, A., Khan, K.A., Ansari, M.J., Almasaudi, S.B., Al-Kahtani, S. (2018). Effect of gut bacterial isolates from Apis mellifera jemenitica on Paenibacillus larvae infected bee larvae. Saudi journal of biological sciences, 25: 383-87.
  • Anjum, S.I., Shah, A.H., Aurongzeb, M., Kori, J., Azim, M.K., Ansari, M.J., Bin, L. (2018). Characterization of gut bacterial flora of Apis mellifera from north-west Pakistan. Saudi journal of biological sciences, 25: 388-92.
  • Cano, R.J., Borucki, M.K., Higby-Schweitzer, M., Poinar, H.N., Poinar Jr, G.O, Pollard KJ, (1994). Bacillus DNA in fossil bees: an ancient symbiosis? Applied and Environmental Microbiology, 60: 2164-67.
  • Chouaia, B., Goda, N., Mazza, G., Alali, S., Florian, F., Gionechetti, F., ... & Montagna, M. (2019). Developmental stages and gut microenvironments influence gut microbiota dynamics in the invasive beetle Popillia japonica Newman (Coleoptera: Scarabaeidae). Environmental microbiology, 21(11), 4343-4359.
  • Corby-Harris, V., Maes, P., Anderson, K.E., (2014). The bacterial communities associated with honey bee (Apis mellifera) foragers. PloS one, 9: e95056.
  • Dal Bello, F., Walter, J., Hertel, C., Hammes, W.P. (2001). In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Systematic and applied microbiology, 24: 232-37
  • Dillon, R.J., Dillon, V., (2004). The gut bacteria of insects: nonpathogenic interactions. Annual Reviews in Entomology, 49: 71-92.
  • Dong, Z.X., Li, H.Y., Chen, Y.F., Wang, F., Deng, X.Y., Lin, L.B., Zhang, Q.L., Li, J.L., Guo, J., (2020). Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiological research, 231: 126370.
  • Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstädter, J., Hurst, G.D. (2008). The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC biology, 6: 1-12.
  • Ellegaard, K.M., Engel, P. (2019). Genomic diversity landscape of the honey bee gut microbiota. Nature communications, 10: 1-13.
  • Ellegaard, K.M., Suenami, S., Miyazaki, R., Engel, P. (2020). Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species. Current biology, 30: 2520-31. e7.
  • Engel, P., Moran, N.A. (2013). The gut microbiota of insects–diversity in structure and function. FEMS microbiology reviews, 37: 699-735.
  • Esawy, M.A., Amer, H., Gamal-Eldeen, A.M., El Enshasy, H.A., Helmy, W.A., Abo-Zeid, M.A., Malek, R., Ahmed, E.F., Awad, G.E. (2013). Scaling up, characterization of levan and its inhibitory role in carcinogenesis initiation stage. Carbohydrate polymers, 95: 578-87
  • Evans, J.D., Armstrong, T.N. (2006). Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC ecology, 6: 1-9.
  • Ganeshprasad, D.N., Lone, J.K., Jani, K., Shouche, Y.S., Khan, K.A., Sayed, S., ... & Sneharani, A. H. (2022). Gut Bacterial Flora of Open Nested Honeybee, Apis florea. Frontiers in Ecology and Evolution, 10.
  • Garrity, G.M., Brenner, D.J., Krieg, N.R., Staley, J.R., & Manual, B.S. (2005). Systematic bacteriology. The Proteobacteria, Part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria, Bergey’s Manual Trust, Department of Microbiology and Molecular Genetics, 2.
  • Gebhardt, K., Schimana, J., Müller, J., Fiedler, H.P., Kallenborn, H.G., Holzenkämpfer, M., Krastel, P., Zeeck, A., Vater, J., Höltzel, A., (2002). Screening for biologically active metabolites with endosymbiotic bacilli isolated from arthropods. FEMS Microbiology Letters, 217: 199-205
  • Gilliam, M., (1997). Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiology Letters, 155: 1-10
  • Gomaa, O.M., Momtaz, O.A., City, N., (2007). 16S rRNA characterization of a Bacillus isolate and its tolerance profile after subsequent subculturing. Arab J Biotech, 10: 107-16.
  • Grady, E.N., MacDonald, J., Liu, L., Richman, A., Yuan, Z.C. (2016). Current knowledge and perspectives of Paenibacillus: a review. Microbial cell factories, 15: 1-18.
  • Hamdy, A.A., Elattal, N.A., Amin, M.A., Ali, A.E., Mansour, N.M., Awad, G.E., Awad, H.M., Esawy, M.A. (2017). Possible correlation between levansucrase production and probiotic activity of Bacillus sp. isolated from honey and honey bee. World Journal of Microbiology and Biotechnology, 33: 1-10.
  • Heslop-Harrison, J. (1968). Pollen wall development: the succession of events in the growth of intricately patterned pollen walls is described and discussed. Science, 161: 230-37.
  • Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A., Werren, J.H. (2008). How many species are infected with Wolbachia?–a statistical analysis of current data. FEMS Microbiology Letters, pp. 215-20.
  • Jones, J.C., Fruciano, C., Hildebrand, F., Al Toufalilia, H., Balfour, N.J., Bork, P., Engel, P., Ratnieks F.L., Hughes, W.O. (2018). Gut microbiota composition is associated with environmental landscape in honey bees. Ecology and evolution, 8: 441-51.
  • Kanzawa, Y., Harada, A., Takeuchi, M., Yokota, A., Harada, T., (1995). Bacillus curdlanolyticus sp. nov. and Bacillus kobensis sp. nov., which hydrolyze resistant curdlan. International Journal of Systematic and Evolutionary Microbiology, 45: 515-21.
  • Kapheim, K.M., Rao, V.D., Yeoman, C.J., Wilson, B.A., White, B.A., Goldenfeld, N., Robinson, G.E. (2015). Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PloS one, 10: e0123911.
  • Khan, K.A., Al-Ghamdi, A.A., Ghramh, H.A., Ansari, M.J., Ali, H., Alamri, S.A., Al-Kahtani, S.N., Adgaba, N., Qasim, M., Hafeez, M. (2020). Structural diversity and functional variability of gut microbial communities associated with honey bees. Microbial pathogenesis, 138: 103793.
  • Khan, K.A., Ansari, M.J., Al-Ghamdi, A., Nuru, A., Harakeh, S., Iqbal, J. (2017). Investigation of gut microbial communities associated with indigenous honey bee (Apis mellifera jemenitica) from two different eco-regions of Saudi Arabia. Saudi journal of biological sciences, 24: 1061-68.
  • Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T., (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the royal society B: biological sciences, 274: 303-13.
  • Kumar, S., Stecher, G., Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular biology and evolution, 33: 1870-74.
  • Ludvigsen, J., Porcellato, D., L'Abée‐Lund, T.M., Amdam, G.V., Rudi, K. (2017). Geographical widespread honeybee‐gut symbiont subgroups show locally distinct antibiotic‐resistant patterns. Molecular ecology, 26: 6590-607.
  • Ludvigsen, J., Rangberg, A., Avershina, E., Sekelja, M., Kreibich, C., Amdam, G., Rudi, K. (2015). Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season. Microbes and environments: ME15019.
There are 33 citations in total.

Details

Primary Language English
Journal Section Moleküler Biyoloji ve Genetik / Moleculer Biology and Genetic
Authors

Mustafa Rustemoglu 0000-0002-1298-1702

Project Number BAP 2019 FNAD 13.02.01
Early Pub Date February 24, 2023
Publication Date March 1, 2023
Submission Date November 15, 2022
Acceptance Date January 3, 2023
Published in Issue Year 2023 Volume: 13 Issue: 1

Cite

APA Rustemoglu, M. (2023). Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record. Journal of the Institute of Science and Technology, 13(1), 592-599. https://doi.org/10.21597/jist.1204926
AMA Rustemoglu M. Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record. J. Inst. Sci. and Tech. March 2023;13(1):592-599. doi:10.21597/jist.1204926
Chicago Rustemoglu, Mustafa. “Gut Bacterial Microbiota of The Honeybee, Apis Mellifera (Hymenoptera: Apidae) With a New Host Record”. Journal of the Institute of Science and Technology 13, no. 1 (March 2023): 592-99. https://doi.org/10.21597/jist.1204926.
EndNote Rustemoglu M (March 1, 2023) Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record. Journal of the Institute of Science and Technology 13 1 592–599.
IEEE M. Rustemoglu, “Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record”, J. Inst. Sci. and Tech., vol. 13, no. 1, pp. 592–599, 2023, doi: 10.21597/jist.1204926.
ISNAD Rustemoglu, Mustafa. “Gut Bacterial Microbiota of The Honeybee, Apis Mellifera (Hymenoptera: Apidae) With a New Host Record”. Journal of the Institute of Science and Technology 13/1 (March 2023), 592-599. https://doi.org/10.21597/jist.1204926.
JAMA Rustemoglu M. Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record. J. Inst. Sci. and Tech. 2023;13:592–599.
MLA Rustemoglu, Mustafa. “Gut Bacterial Microbiota of The Honeybee, Apis Mellifera (Hymenoptera: Apidae) With a New Host Record”. Journal of the Institute of Science and Technology, vol. 13, no. 1, 2023, pp. 592-9, doi:10.21597/jist.1204926.
Vancouver Rustemoglu M. Gut Bacterial Microbiota of The Honeybee, Apis mellifera (Hymenoptera: Apidae) with a New Host Record. J. Inst. Sci. and Tech. 2023;13(1):592-9.