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Bacterial Profile and Fatty Acid Composition of Anatolian Bee Bread Samples by Metataxonomic and Metabolomic Approach

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Abstract

This study investigated the bacterial and postbiotic potential of three Anatolian bee bread samples obtained from different regions of Turkey (Marmara, Aegean, and Mediterranean) and offered for human consumption. The families most commonly found in Anatolian bee bread were Lactobacillaceae, Oscillospiraceae, Bacteroidaceae, Prevotellaceae, and Lachnospiraceae. Lactobacillus delbruckeii was highly abundant, but also other beneficial bacteria, known to be next-generation probiotics, were revealed in bee bread, such as Prevotalla copri, Faecalibacterium prausnitzii, and Akkermansia muciniphila. Apart from these beneficial bacteria, bee bread samples also harbored undesired bacteria such as Phocaeicola vulgatus, Phocaeicola dorei, and Clostridium perfringens. Fatty acid composition showed that bee bread samples had butyric acid, a short-chain fatty acid, as a postbiotic. Additionally, polyunsaturated fatty acids were also found such as alfa-linolenic acid and eicosadienoic acid. The fatty acids with the highest amounts were palmitic acid (~ 30%), stearic acid (~ 17%), and alpha-linolenic acid (~ 12%). One of the samples exhibited antimicrobial activity against Staphylococcus aureus.

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References

  1. Kafantaris I, Amoutzias GD, Mossialos D (2021) Foodomics in bee product research: a systematic literature review. Eur Food Res Technol 247:309–331. https://doi.org/10.1007/s00217-020-03634-5

    Article  CAS  Google Scholar 

  2. Jaya F, Rosyidi D, Radiati LE et al (2020) Antioxidant activity and microbiological quality of bee bread collected from three different species honey bee. IOP Conf Ser Earth Environ Sci. https://doi.org/10.1088/1755-1315/475/1/012033

    Article  Google Scholar 

  3. Barta DG, Cornea-cipcigan M, Margaoan R (2022) Biotechnological processes simulating the natural fermentation process of bee bread and therapeutic properties an overview. Front Nutr. https://doi.org/10.3389/fnut.2022.871896

    Article  PubMed  PubMed Central  Google Scholar 

  4. Zuluaga-Dominguez CM, Fuenmayor CA (2022) Bee bread and gut microbiota. In: Dilek Boyacıoğlu (ed) Bee Products and Their Applications in the Food and Pharmaceutical Industries. Elsevier Inc., 315–345

  5. Mohammad SM, Mahmud-Ab-Rashid NK, Zawawi N (2021) Stingless bee-collected pollen (bee bread): chemical and microbiology properties and health benefits. Molecules 26:1–29. https://doi.org/10.3390/molecules26040957

    Article  CAS  Google Scholar 

  6. Dranca F, Ursachi F, Oroian M (2020) Bee bread: Physicochemical characterization and phenolic content extraction optimization. Foods. https://doi.org/10.3390/foods9101358

  7. Didaras NA, Karatasou K, Dimitriou TG et al (2020) Antimicrobial activity of bee-collected pollen and beebread: State of the art and future perspectives. Antibiotics 9:1–29. https://doi.org/10.3390/antibiotics9110811

    Article  CAS  Google Scholar 

  8. Vásquez A, Olofsson TC (2009) The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res 48:189–195. https://doi.org/10.3896/IBRA.1.48.3.07

    Article  Google Scholar 

  9. Putri SP, Ikram MMM, Sato A et al (2022) Application of gas chromatography-mass spectrometry-based metabolomics in food science and technology. J Biosci Bioeng 133:425–435. https://doi.org/10.1016/j.jbiosc.2022.01.011

    Article  CAS  PubMed  Google Scholar 

  10. Gao Y, Hou L, Gao J et al (2021) Metabolomics approaches for the comprehensive evaluation of fermented foods: a review. Foods 10:1–18. https://doi.org/10.3390/foods10102294

    Article  CAS  Google Scholar 

  11. Kahraman-Ilıkkan Ö, Bağdat EŞ (2022) Metataxonomic sequencing to assess microbial safety of Turkish white cheeses. Brazilian J Microbiol. https://doi.org/10.1007/s42770-022-00730-4

    Article  Google Scholar 

  12. Ilıkkan ÖK, Bağdat EŞ (2021) Comparison of bacterial and fungal biodiversity of Turkish kefir grains with high-throughput metagenomic analysis. Lwt. https://doi.org/10.1016/j.lwt.2021.112375

    Article  Google Scholar 

  13. ISO7889:2003 (2003) Yogurt — Enumeration of characteristic microorganisms. Int Organ Stand

  14. Pełka K, Otłowska O, Worobo RW, Szweda P (2021) Bee bread exhibits higher antimicrobial potential compared to bee pollen. Antibiotics 10:1–14. https://doi.org/10.3390/antibiotics10020125

    Article  CAS  Google Scholar 

  15. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Singh NK, Wood JM, Karouia F, Venkateswaran K (2018) Succession and persistence of microbial communities and antimicrobial resistance genes associated with International Space Station environmental surfaces. Microbiome 6(1):1–23

    Google Scholar 

  17. BioBam Bioinformatics (2022) OmicsBox-Bioinformatics Made Easy Available

  18. Sánchez MC, Valdés A, Velapatiño A et al (2022) Metataxonomic and metabolomic evidence of biofilm homeostasis disruption related to caries: an in vitro study. Mol Oral Microbiol 37(2):81–96. https://doi.org/10.1111/omi.12363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Phillips CD, Phelan G, Dowd SE et al (2012) Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol Ecol 21:2617–2627. https://doi.org/10.1111/j.1365-294X.2012.05568.x

    Article  PubMed  Google Scholar 

  20. Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  21. Engel P, Kwong WK, Moran NA (2013) Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera. Int J Syst Evol Microbiol 63:3646–3651. https://doi.org/10.1099/ijs.0.049569-0

    Article  CAS  PubMed  Google Scholar 

  22. Tully JG, Whitcomb RF, Hackett KJ et al (1998) Entornoplasma freundtii sp. nov., a new species from a green tiger beetle (Coleoptera: Cicindel idae). Int J Syst Bacteriol 48(4):1197–1204

    Article  PubMed  Google Scholar 

  23. Keller A, Brandel A, Becker MC et al (2018) Wild bees and their nests host Paenibacillus bacteria with functional potential of avail. Microbiome 6:1–10. https://doi.org/10.1186/s40168-018-0614-1

    Article  Google Scholar 

  24. Mărgăoan R, Stranț M, Varadi A et al (2019) Bee collected pollen and bee bread: bioactive constituents and health benefits. Antioxidants 8:1–33. https://doi.org/10.3390/antiox8120568

    Article  CAS  Google Scholar 

  25. Silva YP, Bernardi A, Frozza RL (2020) The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol (Lausanne) 11:1–14. https://doi.org/10.3389/fendo.2020.00025

    Article  Google Scholar 

  26. Riwes M, Reddy P (2020) Short chain fatty acids: postbiotics/metabolites and graft versus host disease colitis. Semin Hematol 57:1–6. https://doi.org/10.1053/j.seminhematol.2020.06.001

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kaplan M, Karaoglu Ö, Silici S (2019) An evaluation on bee bread: chemical and palynological analysis. Mellifera 19:21–29

    Google Scholar 

  28. Kaplan M, Karaoglu Ö, Eroglu N, Silici S (2016) Fatty acid and proximate composition of bee bread. Food Technol Biotechnol 54:497–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bakour M, Fernandes Â, Barros L et al (2019) Bee bread as a functional product: chemical composition and bioactive properties. Lwt 109:276–282. https://doi.org/10.1016/j.lwt.2019.02.008

    Article  CAS  Google Scholar 

  30. Human H, Nicolson SW (2006) Nutritional content of fresh, bee-collected and stored pollen of aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67:1486–1492. https://doi.org/10.1016/j.phytochem.2006.05.023

    Article  CAS  PubMed  Google Scholar 

  31. Anderson KE, Carroll MJ, Sheehan T et al (2014) Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol Ecol 23:5904–5917. https://doi.org/10.1111/mec.12966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Abouda Z, Zerdani I, Kalalou I et al (2011) The antibacterial activity of moroccan bee bread and bee-pollen (fresh and dried) against pathogenic bacteria. Res J Microbiol 6:376–384

    Article  Google Scholar 

  33. Urcan A, Criste A, Dezmirean D et al (2018) Antimicrobial activity of bee bread extracts against different bacterial strains. Bull Univ Agric Sci Vet Med Cluj-Napoca Anim Sci Biotechnol 75(2):85. https://doi.org/10.15835/buasvmcn-asb:2018.0004

    Article  CAS  Google Scholar 

  34. Muñoz-Colmenero M, Baroja-Careaga I, Kovačić M et al (2020) Differences in honey bee bacterial diversity and composition in agricultural and pristine environments – a field study. Apidologie 51:1018–1037. https://doi.org/10.1007/s13592-020-00779-w

    Article  Google Scholar 

  35. Disayathanoowat T, Li H, Supapimon N et al (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. https://doi.org/10.3390/microorganisms8020264

    Article  PubMed  PubMed Central  Google Scholar 

  36. Bakour M, Laaroussi H, Ousaaid D et al (2022) Bee bread as a promising source of bioactive molecules and functional properties: an up-to-date review. Antibiotics 11:1–39. https://doi.org/10.3390/antibiotics11020203

    Article  CAS  Google Scholar 

  37. Iorizzo M, Pannella G, Lombardi SJ et al (2020) Inter-and intra-species diversity of lactic acid bacteria in apis mellifera ligustica colonies. Microorganisms 8:1–17. https://doi.org/10.3390/microorganisms8101578

    Article  CAS  Google Scholar 

  38. Huang F, Sardari RRR, Jasilionis A et al (2021) Cultivation of the gut bacterium Prevotella copri DSM 18205T using glucose and xylose as carbon sources. Microbiologyopen 10:1–15. https://doi.org/10.1002/mbo3.1213

    Article  CAS  Google Scholar 

  39. Khan MT, Duncan SH, Stams AJM et al (2012) The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic-anoxic interphases. ISME J 6:1578–1585. https://doi.org/10.1038/ismej.2012.5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Maioli TU, Borras-Nogues E, Torres L et al (2021) Possible benefits of faecalibacterium prausnitzii for obesity-associated gut disorders. Front Pharmacol 12:1–13. https://doi.org/10.3389/fphar.2021.740636

    Article  CAS  Google Scholar 

  41. Cani PD, Depommier C, Derrien M et al (2022) Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat Rev Gastroenterol Hepatol. https://doi.org/10.1038/s41575-022-00631-9

    Article  PubMed  Google Scholar 

  42. Cobo F, Peerez-Carrasco V, Rodríguez-Guerrero E et al (2022) Misidentification of Phocaeicola (Bacteroides) dorei in two patients with bacteremia. Anaerobe 75:6–8. https://doi.org/10.1016/j.anaerobe.2022.102544

    Article  Google Scholar 

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Acknowledgements

The author would like to thank Isparta University of Applied Sciences, Research Center for the FAME analysis. This study was performed in Başkent University Food Processing Laboratory.

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The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

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  1. Department of Food Processing, Başkent University, 06980, Ankara, Turkey

    Özge Kahraman-Ilıkkan

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OKI: design of experiment, analyses, and interpretation of all experiments, writing of the manuscript.

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Correspondence to Özge Kahraman-Ilıkkan.

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Kahraman-Ilıkkan, Ö. Bacterial Profile and Fatty Acid Composition of Anatolian Bee Bread Samples by Metataxonomic and Metabolomic Approach. Curr Microbiol 80, 90 (2023). https://doi.org/10.1007/s00284-023-03195-2

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