Insights into the gut microbiome of local steppe-vegetation inhabitant bees: microbial community analysis of Bombus niveatus niveatus, Bombus niveatus vorticosus, Bombus terrestris, and Apis mellifera

References

• Abduljalil, J. M., & Abd Al Galil, F. M. (2022). Molecular pathogenesis of dengue virus infection in Aedes mosquitoes. Journal of Insect Physiology, 138, 104367. https://doi.org/10.1016/j.jinsphys.2022.104367
   PubMed Web of Science ®Google Scholar
• Abou-Shaara, H. F., Owayss, A. A., Ibrahim, Y. Y., & Basuny, N. K. (2017). A review of impacts of temperature and relative humidity on various activities of honey bees. Insectes Sociaux, 64(4), 455–463. https://doi.org/10.1007/s00040-017-0573-8
   Web of Science ®Google Scholar
• Akaydın, G. (2011). Beytepe bitkileri. Hacettepe Üniversitesi Basımevi.
   Google Scholar
• Aldercotte, A. H., Simpson, D. T., & Winfree, R. (2022). Crop visitation by wild bees declines over an 8‐year time series: A dramatic trend, or just dramatic between‐year variation? Insect Conservation and Diversity, 15(5), 522–533. https://doi.org/10.1111/icad.12589
   Web of Science ®Google Scholar
• Backhed, F. (2005). Host-bacterial mutualism in the human intestine. Science, 307, 1920. https://doi.org/10.1126/science.1104816
   PubMed Web of Science ®Google Scholar
• Barretto, D. A., Gadwala, M., & Vootla, S. K. (2021). The silkworm gut microbiota: A potential source for biotechnological applications (Chapter 1). Elsevier.
   Google Scholar
• Beribaka, M., Jelić, M., Tanasković, M., Lazić, C., & Stamenković-Radak, M. (2021). Life history traits in two drosophila species differently affected by microbiota diversity under lead exposure. Insects, 12(12), 1122. https://doi.org/10.3390/insects12121122
   PubMed Web of Science ®Google Scholar
• Brysch-Herzberg, M. (2004). Ecology of yeasts in plant–bumblebee mutualism in Central Europe. FEMS Microbiology Ecology, 50(2), 87–100. https://doi.org/10.1016/j.femsec.2004.06.003
   PubMed Web of Science ®Google Scholar
• Colla, S. R. (2022). The potential consequences of ‘bee washing’on wild bee health and conservation. International Journal for Parasitology. Parasites and Wildlife, 18, 30–32. https://doi.org/10.1016/j.ijppaw.2022.03.011
   PubMed Web of Science ®Google Scholar
• Coulibaly, K. A., Majeed, M. Z., Sayed, S., & Yeo, K. (2022). Simulated climate warming influenced colony microclimatic conditions and gut bacterial abundance of honeybee subspecies and A. mellifera sinisxinyuan. Journal of Apicultural Science, 66(1), 15–27. https://doi.org/10.2478/jas-2022-0002
   Web of Science ®Google Scholar
• Disayathanoowat, T., Li, H., Supapimon, N., Suwannarach, N., Lumyong, S., Chantawannakul, P., & Guo, J. (2020). Different dynamics of bacterial and fungal communities in hive-stored bee bread and their possible roles: A case study from two commercial honey bees in China. Microorganisms, 8(2), 264. https://doi.org/10.3390/microorganisms8020264
   PubMed Web of Science ®Google Scholar
• Ellegaard, K. M., Tamarit, D., Javelind, E., Olofsson, T. C., Andersson, S. G., & Vásquez, A. (2015). Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics, 16(1), 1–22. https://doi.org/10.1186/s12864-015-1476-6
   PubMedGoogle Scholar
• 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. https://doi.org/10.1073/pnas.1202970109
   PubMed Web of Science ®Google Scholar
• Engel, P., & Moran, N. A. (2013). The gut microbiota of insects–diversity in structure and function. FEMS Microbiology Reviews, 37(5), 699–735. https://doi.org/10.1111/1574-6976.12025
   PubMed Web of Science ®Google Scholar
• Erik, S. (1994). Beytepe Kampüsü (Ankara) Florası. Hacettepe Fen ve Mühendislik Fakültesi Dergisi Seri A, 15, 49–109.
   Google Scholar
• Gilliam, M., & Prest, D. B. (1977). The mycoflora of selected organs of queen honey bees, Apis mellifera. Journal of Invertebrate Pathology, 29(2), 235–237. https://doi.org/10.1016/0022-2011(77)90201-4
   Web of Science ®Google Scholar
• Goulson, D. (2003). Bumblebees: Their behaviour and ecology. Oxford University Press.
   Google Scholar
• Hammer, T. J., Le, E., Martin, A. N., & Moran, N. A. (2021). The gut microbiota of bumblebees. Insectes Sociaux, 68(4), 287–301. https://doi.org/10.1007/s00040-021-00837-1
   PubMed Web of Science ®Google Scholar
• Jang, S., & Kikuchi, Y. (2020). Impact of the insect gut microbiota on ecology, evolution, and industry. Current Opinion in Insect Science, 41, 33–39. https://doi.org/10.1016/j.cois.2020.06.004
   PubMed Web of Science ®Google Scholar
• Kadoguchi, H., Hori, A., & Kuraishi, T. (2022). Gut microbes and Drosophila behavior. Behavioral neurogenetics (pp. 57–75). Humana.
   Google Scholar
• Klein, A. M., Boreux, V., Fornoff, F., Mupepele, A. C., & Pufal, G. (2018). Relevance of wild and managed bees for human well-being. Current Opinion in Insect Science, 26, 82–88. https://doi.org/10.1016/j.cois.2018.02.011
   PubMed Web of Science ®Google Scholar
• Klungness, L. M., & Peng, Y. S. (1984). A histochemical study of pollen digestion in the alimentary canal of honeybees (Apis mellifera L.). Journal of Insect Physiology, 30(7), 511–521. https://doi.org/10.1016/0022-1910(84)90077-5
   Web of Science ®Google Scholar
• Koch, H., Abrol, D. P., Li, J., & Schmid‐Hempel, P. (2013). Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Molecular Ecology, 22(7), 2028–2044. https://doi.org/10.1111/mec.12209
   PubMed Web of Science ®Google Scholar
• Krams, R., Gudra, D., Popovs, S., Willow, J., Krama, T., Munkevics, M., Megnis, K., Jõers, P., Fridmanis, D., Garduño, J. C., & Krams, I. A. (2022). Dominance of Fructose-Associated Fructobacillus in the Gut Microbiome of Bumblebees (Bombus terrestris) Inhabiting Natural Forest Meadows. Insects, 13(1), 98. https://doi.org/10.3390/insects13010098
   PubMed Web of Science ®Google Scholar
• Kwong, W. K., Engel, P., Koch, H., & Moran, N. A. (2014). Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences, 111(31), 11509–11514. https://doi.org/10.1073/pnas.1405838111
   PubMed Web of Science ®Google Scholar
• Kwong, W. K., Medina, L. A., Koch, H., Sing, K. W., Soh, E. J. Y., Ascher, J. S., Jaffé, R., & Moran, N. A. (2017). Dynamic microbiome evolution in social bees. Science Advances, 3(3), e1600513. https://doi.org/10.1126/sciadv.1600513
   PubMed Web of Science ®Google Scholar
• Le Conte, Y., & Navajas, M. (2008). Climate change: Impact on honey bee populations and diseases. Revue Scientifique et Technique-Office International Des Epizooties, 27(2), 499–510.
   Web of Science ®Google Scholar
• Lee, F. J., Rusch, D. B., Stewart, F. J., Mattila, H. R., & Newton, I. L. (2015). Saccharide breakdown and fermentation by the honey bee gut microbiome. Environmental Microbiology, 17(3), 796–815. https://doi.org/10.1111/1462-2920.12526
   PubMed Web of Science ®Google Scholar
• Liczner, A. R., & Colla, S. R. (2019). A systematic review of the nesting and overwintering habitat of bumble bees globally. Journal of Insect Conservation, 23(5–6), 787–801. https://doi.org/10.1007/s10841-019-00173-7
   Web of Science ®Google Scholar
• Ma, M., Chen, X., Li, S., Luo, J., Han, R., & Xu, L. (2023). Composition and diversity of gut bacterial community in different life stages of a leaf beetle Gastrolina depressa. Microbial Ecology, 86(1), 590–600. https://doi.org/10.1007/s00248-022-02054-0
   PubMed Web of Science ®Google Scholar
• Malacrinò, A. (2022). Host species identity shapes the diversity and structure of insect microbiota. Molecular Ecology, 31(3), 723–735. https://doi.org/10.1111/mec.16285
   PubMed Web of Science ®Google Scholar
• Mockler, B. K., Kwong, W. K., Moran, N. A., & Koch, H. (2018). Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Applied and Environmental Microbiology, 84(7), e02335–17. https://doi.org/10.1128/AEM.02335-17
   PubMed Web of Science ®Google Scholar
• Mutlu, B., Sadık, E., & Tarıkahya, B. (2008). New contributions to the flora of Beytepe Campus Ankara and floristic comparison with neighboring floras and other campus floras. Hacettepe Journal of Biology and Chemistry, 36(3), 181–195.
   Google Scholar
• Neish, A. S. (2009). Microbes in gastrointestinal health and disease. Gastroenterology, 136(1), 65–80. https://doi.org/10.1053/j.gastro.2008.10.080
   PubMed Web of Science ®Google Scholar
• Öksüzoğlu, D., & Aydın, M. (2022). Ecological niche modeling: An empirical study on Apis mellifera population distribution. Uludağ Arıcılık Dergisi, 22(1), 31–44. https://doi.org/10.31467/uluaricilik.1075065
   Google Scholar
• Ollerton, J. (2017). Pollinator diversity: Distribution, ecological function, and conservation. Annual Review of Ecology, Evolution, and Systematics, 48(1), 353–376. https://doi.org/10.1146/annurev-ecolsys-110316-022919
   Web of Science ®Google Scholar
• Özbek, H. (1983). Doğu Anadolu’nun bazı yörelerindeki Bombinae (Hymenoptera;Apoidea,Bombidae) türleri üzerinde taksonomik ve bazı biyolojik çalışmalar. Atatürk Üniversitesi Basimevi.
   Google Scholar
• Papp, M., Békési, L., Farkas, R., Makrai, L., Judge, M. F., Maróti, G., Tőzsér, D., & Solymosi, N. (2022). Natural diversity of the honey bee (Apis mellifera) gut bacteriome in various climatic and seasonal states. PLoS One, 17(9), e027384. https://doi.org/10.1371/journal.pone.0273844
   Web of Science ®Google Scholar
• Pimentel, M. R., Antonini, Y., Martins, R. P., Lachance, M. A., & Rosa, C. A. (2005). Candida riodocensis and Candida cellae, two new yeast species from the Starmerella clade associated with solitary bees in the Atlantic rain forest of Brazil. FEMS Yeast Research, 5(9), 875–879. https://doi.org/10.1016/j.femsyr.2005.03.006
   PubMed Web of Science ®Google Scholar
• Ptaszyńska, A. A., Latoch, P., Hurd, P. J., Polaszek, A., Michalska-Madej, J., Grochowalski, Ł., Strapagiel, D., Gnat, S., Załuski, D., Gancarz, M., Rusinek, R., Krutmuang, P., Martín Hernández, R., Higes Pascual, M., & Starosta, A. L. (2021). Amplicon sequencing of variable 16s rRNA from bacteria and ITS2 regions from fungi and plants, reveals honeybee susceptibility to diseases results from their forage availability under anthropogenic landscapes. Pathogens, 10(3), 381. https://doi.org/10.3390/pathogens10030381
   PubMed Web of Science ®Google Scholar
• Rasmont, P., Aytekin, A. M., Kaftanoğlu, O., Flagothier, D. (2009). The bumblebees of Turkey. Atlas Hymenoptera, Université de Mons, Gembloux Agro-Biotech. http://www.atlashymenoptera.net/page.aspx??ID=103
   Google Scholar
• Rasmont, P., Iserbyt, I. (2010–2014). Atlas of the European bees: Genus bombus (3rd ed.). STEP Project, Atlas Hymenoptera. http://www.atlashymenoptera.net/page.aspx?ID=169
   Google Scholar
• Rasmont, P., Terzo, M., Aytekin, A. M., Hines, H., Urbanova, K., Cahlikova, L., & Valterova, I. (2005). Cephalic secretions of the bumblebee subgenus Sibiricobombus Vogt suggest Bombus niveatus Kriechbaumer and Bombus vorticosus Gerstaecker are conspecific (Hymenoptera, Apidae, Bombus). Apidologie, 36(4), 571–584. https://doi.org/10.1051/apido:2005047
   Web of Science ®Google Scholar
• 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. https://doi.org/10.1016/j.cois.2018.02.012
   PubMed Web of Science ®Google Scholar
• Rothman, J. A., Leger, L., Graystock, P., Russell, K., & McFrederick, Q. S. (2019). The bumble bee microbiome increases survival of bees exposed to selenate toxicity. Environmental Microbiology, 21(9), 3417–3429. https://doi.org/10.1111/1462-2920.14641
   PubMed Web of Science ®Google Scholar
• Şahin, M. K., Akbaba, B., Bulut, Ş., & Zafer, A. (2021). The checklist of terrestrial vertebrate fauna of Beytepe Campus, Hacettepe University. Hacettepe Journal of Biology and Chemistry, 49(1), 43–55. https://doi.org/10.15671/hjbc.722876
   Google Scholar
• Shehabeldine, A. M., Hashem, A. H., & Hasaballah, A. I. (2022). Antagonistic effect of gut microbiota of the Egyptian honeybees, Apis mellifera L. against the etiological agent of Stonebrood disease. International Journal of Tropical Insect Science, 42(2), 1357–1366. https://doi.org/10.1007/s42690-021-00654-w
   Web of Science ®Google Scholar
• Shi, X., Zhang, Y., Zhu, T., Li, N., Sun, S., Zhu, M., Pan, J., Shen, Z., Hu, X., Zhang, X., & Gong, C. (2021). Response to Bombyx mori nucleopolyhedrovirus infection in silkworm: Gut metabolites and microbiota. Developmental and Comparative Immunology, 125, 104227. https://doi.org/10.1016/j.dci.2021.104227
   PubMed Web of Science ®Google Scholar
• Singh, A., Allam, M., Kwenda, S., Khumalo, Z. T., Ismail, A., & Oliver, S. V. (2022). The dynamic gut microbiota of zoophilic members of the Anopheles gambiae complex (Diptera: Culicidae). Scientific Reports, 12(1), 1495. https://doi.org/10.1038/s41598-022-05437-y
   PubMed Web of Science ®Google Scholar
• Stefanini, I. (2018). Yeast‐insect associations: It takes guts. Yeast (Chichester, England), 35(4), 315–330. https://doi.org/10.1002/yea.3309
   PubMed Web of Science ®Google Scholar
• Subotic, S., Boddicker, A. M., Nguyen, V. M., Rivers, J., Briles, C. E., & Mosier, A. C. (2019). Honey bee microbiome associated with different hive and sample types over a honey production season. PLoS One, 14(11), e0223834. https://doi.org/10.1371/journal.pone.0223834
   PubMed Web of Science ®Google Scholar
• Thursby, E., & Juge, N. (2017). Introduction to the human gut microbiota. The Biochemical Journal, 474(11), 1823–1836. https://doi.org/10.1042/BCJ20160510
   PubMed Web of Science ®Google Scholar
• Töre, D., & Erik, S. (2012). The flora of bağlıca campus of Başkent University (Ankara). Hacettepe Journal of Biology & Chemistry, 40(3), 267–291.
   Google Scholar
• Vieco-Saiz, N., Belguesmia, Y., Raspoet, R., Auclair, E., Gancel, F., Kempf, I., & Drider, D. (2019). Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Frontiers in Microbiology, 10, 57. https://doi.org/10.3389/fmicb.2019.00057
   PubMed Web of Science ®Google Scholar
• Wang, H., Xian, X., Gu, Y., Castañé, C., Arnó, J., Wu, S., Wan, F., Liu, W., Zhang, G., & Zhang, Y. (2022). Similar bacterial communities among different populations of a newly emerging invasive species, Tuta absoluta (Meyrick). Insects, 13(3), 252. https://doi.org/10.3390/insects13030252
   PubMed Web of Science ®Google Scholar
• Weidenmüller, A., Kleineidam, C., & Tautz, J. (2002). Collective control of nest climate parameters in bumblebee colonies. Animal Behaviour, 63(6), 1065–1071. https://doi.org/10.1006/anbe.2002.3020
   Google Scholar
• Williams, P. H. (2021). Not just cryptic, but a barcode bush: PTP re-analysis of global data for the bumblebee subgenus Bombus s. str. supports additional species (Apidae, genus Bombus). Journal of Natural History, 55(5–6), 271–282. https://doi.org/10.1080/00222933.2021.1900444
   Web of Science ®Google Scholar
• Williams, P. H., Cameron, S. A., Hines, H. M., Cederberg, B., & Rasmont, P. (2008). A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie, 39(1), 46–74. https://doi.org/10.1051/apido:2007052
   Web of Science ®Google Scholar
• Zattara, E. E., & Aizen, M. A. (2021). Worldwide occurrence records suggest a global decline in bee species richness. One Earth, 4(1), 114–123. https://doi.org/10.1016/j.oneear.2020.12.005
   Google Scholar
• Zhang, J., Chen, C., Zhu, K., Ma, H., Fu, Z., Tan, H., & Wang, X. (2022). Variation in gut microbial communities of Chilo suppressalis in the typical bivoltine areas of northern China. Journal of Applied Entomology, 146(7), 860–874. https://doi.org/10.1111/jen.13016
   Web of Science ®Google Scholar
• Zhang, Z., Mu, X., Cao, Q., Shi, Y., Hu, X., & Zheng, H. (2022). Honeybee gut Lactobacillus modulates host learning and memory behaviors via regulating tryptophan metabolism. Nature Communications, 13(1), 2037. https://doi.org/10.1038/s41467-022-29760-0
   PubMed Web of Science ®Google Scholar
• Zhang, X., Zhang, F., & Lu, X. (2022). Diversity and Functional Roles of the Gut Microbiota in Lepidopteran Insects. Microorganisms, 10(6), 1234. https://doi.org/10.3390/microorganisms10061234
   PubMed Web of Science ®Google Scholar
• Zheng, H., Nishida, A., Kwong, W. K., Koch, H., Engel, P., Steele, M. I., & Moran, N. A. (2016). Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. mBio, 7(6), e01326. https://doi.org/10.1128/mBio.01326-16
   PubMed Web of Science ®Google Scholar