Abstract
Lactic acid bacteria and bifidobacteria (LAB and Bifido), isolated from the gastrointestinal tract of Apis mellifera intermissa (BGIT), honey (H), propolis (P) and bee bread (BB) of hives set in different vegetations (wildflowers, caraway, orange blossom, Marrubium vulgare, Eucalyptus and Erica cinerea), were subjected to analysis of their antibacterial potential. Isolates able to inhibit Staphylococcus aureus were selected and identified with MALDI-TOF MS leading to 154 strains representing 12 LAB and Bifido species. Lactiplantibacillus plantarum, Pediococcus pentosaceus and Enterococcus faecalis were predominantly found in all matrices. BGIT showed the highest LAB and Bifido diversity with exclusive occurrences of five species (including Bifidobacterium asteroides and Limosilactobacillus fermentum). Honey was the second origin harboring an important variety of LAB species of which Apilactobacillus kunkeei and Enterococcus mundtii were characteristic of both H and BGIT. Principal components analysis revealed associations between antibacterial activities of LAB and Bifido, matrices and honey bee forage plants. Inhibition trends of S. aureus and Citrobacter freundii were highlighted with: L. plantarum from BGIT, P, H of bees feeding on E. cinerea; Pediococcus pentosaceus from BGIT, P, BB associated with E. cinerea; and Bifidobacterium asteroides from BGIT/orange blossom system. However, Enterococcus faecium associated with BGIT/Eucalyptus system antagonized Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa and Acinetobacter baumannii. Our findings highlighted noteworthy effects of bee forage plants on the antibacterial activity of LAB and Bifido. Our approach could be useful to identify multiple conditions promoting antibacterial potency of LAB and Bifido under the combined effects of feeding plants and living matrices.
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Acknowledgements
We thank Pr. Karim Naghmouchi, from Biochemistry and Biotechnology Laboratory, Faculty of Sciences of Tunis, University of Tunis El Manar and College of Clinical Pharmacy, Department of Pharmaceutical Chemistry, Al Baha University, Saudi Arabia, for suggesting us to investigate LAB and Bifido from honey bee; Dr. Lamia Thabet, from Traumatology and Great Burned Center, Tunis, Tunisia, for the gift of strains S. aureus, E. coli, K. pneumoniae, A. baumannii, C. freundii and P. aeruginosa (collection of 2018). MALDI-TOF MS experiment was performed at the Department of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal.
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The authors are grateful to The Tunisian Ministry of Higher Education and Scientific Research for financial support for the laboratory LR01ES05. The funder had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
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HB-M designed the study, performed experiments and drafted the manuscript. NS realized the statistical analysis (distribution analysis, principal component analysis) of antibacterial activity and contributed to the manuscript writing and revision. MSC completed biostatistical analyses and contributed to manuscript writing. KB-M contributed to the manuscript revision. M-OB-B. contributed to study supervision, and manuscript writing and edition. SR supervised the work, wrote and edited the manuscript. All authors reviewed the manuscript.
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Ben-Miled, H., Semmar, N., Castellanos, M.S. et al. Effect of honey bee forage plants in Tunisia on diversity and antibacterial potential of lactic acid bacteria and bifidobacteria from Apis mellifera intermissa and its products. Arch Microbiol 205, 295 (2023). https://doi.org/10.1007/s00203-023-03630-9
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DOI: https://doi.org/10.1007/s00203-023-03630-9