Isolation and Antimicrobial Susceptibility of Some Bacteria From The Gut of Honey Bees in Siirt Province of Türkiye

Yıl 2024, Cilt: 13 Sayı: 1, 47 - 54, 28.06.2024

Özgül Gülaydın , Mustafa Kahyaoğlu , Ali Gülaydın

https://doi.org/10.53913/aduveterinary.1413768

Öz

Bu çalışmada, Siirt ili ve yöresinde bulunan bal arılarının bağırsak içeriklerinden bazı aerobik bakterilerin varlığı araştırıldı. Bakteriyel etkenler konvansiyonel bakteriyolojik yöntemlerle izole edildi ve ticari identifikasyon test kiti ile identifiye edildi. İzolatların antimikrobiyal duyarlılığı disk difüzyon testi ile belirlendi. Çalışmada en yüksek oranda izole edilen etkenlerin Staphylococcus spp. ve Klebsiella spp. olduğu ve bunu sırasıyla Bacillus spp. Izolatlarının izlediği belirlendi. GSBL ve plasmidik AmpC direnci 12 adet Gram negatif etkenin 6 (%50)’sında tespit edildi. Ayrıca Enterobacteriaceae izolatlarında imipenem direncinin yüksek olduğu belirlendi. Buna karşın Staphylococcus spp. izolatlarının çalışmada kullanılan antimikrobiyal maddelerin çoğuna duyarlı olduğu görüldü. Çalışmadan elde edilen verilerin bal arıları ile ilgili yapılan çalışmalara katkı sağlayacağı düşünüldü.

Anahtar Kelimeler

honey bee, bacteria, antimicrobial susceptibility

Etik Beyan

The study was approved by the Siirt University Animal Experiments Local Ethics Committee with the number of 2021/01/02.

Proje Numarası

This work was supported by the Siirt University Agriculture and Livestock Specialization Coordination Center with the project number of 2022-IHTVET-02.

Siirt İli ve Yöresindeki Bal Arılarının Bağırsak İçeriklerinden Bazı Bakteriyel Etkenlerin İzolasyonu ve Antimikrobiyal Duyarlılıkları

Öz

Bu çalışmada, Siirt ili ve yöresinde bulunan bal arılarının bağırsak içeriklerinden bazı aerobik bakterilerin varlığı araştırıldı. Bakteriyel etkenler konvansiyonel bakteriyolojik yöntemlerle izole edildi ve ticari identifikasyon test kiti ile identifiye edildi. İzolatların antimikrobiyal duyarlılığı disk difüzyon testi ile belirlendi. Çalışmada en yüksek oranda izole edilen etkenlerin Staphylococcus spp. ve Klebsiella spp. olduğu ve bunu sırasıyla Bacillus spp. Izolatlarının izlediği belirlendi. GSBL ve plasmidik AmpC direnci 12 adet Gram negatif etkenin 6 (%50)’sında tespit edildi. Ayrıca Enterobacteriaceae izolatlarında imipenem direncinin yüksek olduğu belirlendi. Buna karşın Staphylococcus spp. izolatlarının çalışmada kullanılan antimikrobiyal maddelerin çoğuna duyarlı olduğu görüldü. Çalışmadan elde edilen verilerin bal arıları ile ilgili yapılan çalışmalara katkı sağlayacağı düşünüldü.

Anahtar Kelimeler

Bal arısı, bakteri, antimikrobiyal duyarlılık

Proje Numarası

This work was supported by the Siirt University Agriculture and Livestock Specialization Coordination Center with the project number of 2022-IHTVET-02.

Kaynakça

• Aslantaş, Ö., & Yılmaz, E.Ş. (2017). Prevalence and molecular characterization of extended-spectrum β-lactamase (ESBL) and plasmidic AmpC β-lactamase (pAmpC) producing Escherichia coli in dogs. The Journal of Veterinary Medical Science, 79, 1024-1030. https://doi.org/10.1292/jvms.16-0432
• Baffoni, L., Alberoni, D., Gaggìa, F., Braglia, C., Stanton, C., Ross, P.R., &Di Gioia, D. (2021). Honeybee exposure to veterinary drugs: how is the gut microbiota affected? Microbiology Spectrum, 9(1), e00176-21. https://doi.org/10.1128/spectrum.00176-21
• Berry, D.B., Lu, D., Geva, M., Watts, J.C., Bhardwaj, S., Oehler, A., Renslo, A.R., DeArmond, S.J., Prusiner, S.B., & Giles, K. (2013). Drug resistance confounding prion therapeutics. Proceedings of the National Academy of Sciences of the United States of America, 110, 4160-4169. https://doi.org/10.1073/pnas.1317164110
• Boğ, E.Ş., Ertürk, Ö., & Yaman, M. (2020). Pathogenicity of aerobic bacteria isolated from honeybees (Apis mellifera) in Ordu Province. Turkish Journal of Veterinary and Animal Sciences, 44(3), 714-719. https://doi.org/10.3906/vet-1905-67
• Campanella, T.A., & Gallagher, J.C. (2020). A clinical review and critical evaluation of imipenem-relebactam: evidence to date. Infection and drug resistance, 13, 4297-4308. https://doi.org/10.2147/IDR.S224228
• Cenci-Goga, B.T., Sechi, P., Karama, M., Ciavarella, R., Pipistrelli, M.V., Goretti, E., Elia, A.C., Gardi, T., Pallottini, M., Rossi, R., Selvaggi, R. & Grispoldi, L. (2020). Cross-sectional study to identify risk factors associated with the occurrence of antimicrobial resistance genes in honey bees Apis mellifera) in Umbria, Central Italy. Environmental Science Pollution Research, 27, 9637-9645. https://doi.org/10.1007/s11356-020-07629-3
• Christaki, E., Marcou, M., & Tofarides, A. (2019). Antimicrobial resistance in bacteria: mechanisms, evolution, and persistence. Journal of Molecular Evolution, 881(88), 26-40. https://doi.org/10.1007/s00239-019-09914-3
• Cilia, G., Fratini, F., Tafi, E., Mancini, S., Turchi, B., Sagona, S., Cerri, D., Felicioli, A., & Nanetti, A. (2020). Changes of Western honey bee Apis mellifera ligustica (Spinola, 1806) ventriculus microbial profile related to their in-hive tasks. Journal of Apicultural Research, 60(1), 198-202. https://doi.org/10.1080/00218839.2020.1830259
• Cilia, G., Bortolotti, L. Albertazzi, S., Ghini, S., & Nanetti, A. (2022). Honey bee (Apis mellifera L.) colonies as bioindicators of environmental SARS-CoV-2 occurrence. Science of the Total Environment, 805, 150327. https://doi.org/10.1016/j.scitotenv.2021.150327
• Clinical Laboratory Standart Institute: Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals. 4th ed., Vet 08. Wayne, PA: CLSI, 2018.
• Dang, T., Loll, B., Müller, S., Skobalj, R., Ebeling, J., Bulatov, T., Gensel, S., Gobel, J., Wahl, M.C., Genersch, E., Mainz, A., & Süssmuth, R.D. (2022). Molecular basis of antibiotic self-resistance in a bee larvae pathogen. Nature Communications, 131(13), 1-11. https://doi.org/10.1038/s41467-022-29829
• Disayathanoowat, T., Yoshiyama, M., Kimura, K., & Chantawannakul, P. (2012). Isolation and characterization of bacteria from the midgut of the Asian honey bee (Apis cerana indica). Journal of Apicultural Research, 51(4), 312-319. https://doi.org/10.3896/IBRA.1.51.4.04
• Ebrahimi, A., & Lotfalian, Sh. (2005). Isolation and antibiotic resistance patterns of Escherichia coli and coagulase-positive Staphylococcus aureus from honey bees digestive tract. Iranian Journal of Veterinary Research, 6(2), 51-53.
• European Committee on Antimicrobial Susceptibility Testing (EUCAST): Clinical Breakpoint Tables v. 9.0, valid from 2019-01-01.
• Evans, J.D. (2003). Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. Journal of Invertebrate Pathology, 83(1), 46-50. https://doi.org/10.1016/S0022-2011(03)00039-9.
• Gilliam, M. (1997). Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiology Letters, 155(1), 1-10. https://doi.org/10.1111/j.1574-6968.1997.tb12678.x
• Gumus, B., Celık, B., Kahraman, B.B., Sıgırcı, B.D., & Ak, S. (2017). Determination of extended-spectrum beta-lactamase (ESBL) and AmpC beta-lactamase-producing Escherichia coli prevalence in fecal samples of healthy dogs and cats. Revue de Medecine Veterinaire, 168 (1-3), 46-52.
• Gwenzi, W., Chaukura, N., Muisa-Zikali, N., Teta, C., Musvuugwa, T., Rzymski, P., & Abia, A.L.K. (2021). Insects, rodents, and pets as reservoirs, vectors, and sentinels of antimicrobial resistance. Antibiotics, 10(1), 68. https://doi.org/10.3390/antibiotics10010068
• Ignasiak, K., & Maxwell, A. (2017). Antibiotic-resistant bacteria in the guts of insects feeding on plants: prospects for discovering plantderived antibiotics. BMC Microbiology, 17, 1-17. https://doi.org/10.1186/s12866-017-1133-0
• Kaplan, B., & Gulaydin, O. (2023). Characterization of extendedspectrum β-lactamase producing Escherichia coli strains isolated from the urogenital system of dogs in Van province of Turkey. Iranian Journal of Veterinary Research, 24(1), 22-29. https://doi.org/10.22099/IJVR.2022.43280.6301
• Koeniger, G., Koeniger, N., & Fabritius, M. (2015). Some detailed observations of mating in the honeybee. Bee World, 60(2), 53-57. https://doi.org/10.1080/0005772X.1979.11097736
• Kok, M., Maton, L., van der Peet, M., Hankemeier, T., & van Hasselt, J.G.C. (2022). Unraveling antimicrobial resistance using metabolomics. Drug Discovery Today, 27(6), 1774-1783. https://doi.org/10.1016/J.DRUDIS.2022.03.015.
• Krongdang, S., Evans, J.D., Pettis, J.S., & Chantawannakul, P. (2017). Multilocus sequence typing, biochemical and antibiotic resistance characterizations reveal diversity of North American strains of the honey bee pathogen Paenibacillus larvae. PLoS One, 12, e0176831. https://doi.org/10.1371/JOURNAL.PONE.0176831.
• Laconi, A Tolosi, R. Mughini-Gras, L., Mazzuccato, M., Ferr`e, N., Capolongo, F., Merlanti, R., & Piccirillo, A. (2022). Beehive products as bioindicators of antimicrobial resistance contamination in the environment. Science of the Total Environment, 823, 151131. https://doi.org/10.1016/J.SCITOTENV.2021.151131
• Ludvigsen, J., Amdam, G.V., Rudi, K., & L’Ab´ee-Lund, T.M. (2018). Detection and characterization of streptomycin resistance (strAstrB) in a honeybee gut symbiont (Snodgrassella alvi) and the associated risk of antibiotic resistance transfer. Microbial Ecology, 76, 588-591. https://doi.org/10.1007/S00248-018-1171-7
• Ludvigsen, J., Porcellato, D., L’Ab´ee-Lund, T.M., Amdam, G.V., & Rudi, K. (2017). Geographically widespread honeybee-gut symbiont subgroups show locally distinct antibiotic-resistant patterns. Molecular Ecology, 26(23), 6590-6607. https://doi.org/10.1111/MEC.14392
• Lyapunov, Y.E., Kuzyaev, R.Z., Khismatullin, R.G., & Bezgodova, O.A. (2008). Intestinal enterobacteria of the hibernating Apis mellifera mellifera L. bees. Microbiology, 77(3), 373-379. https://doi.org/0.1134/S0026261708030181
• Maluta, R.P., Stella, A.E., Riccardi, K., Rigobelo, E.C., Marin, J.M., Carvalho, M.B., & Ávila, F.A.D. (2012). Phenotypical characterization and adhesin identification in Escherichia coli strains isolated from dogs with urinary tract infections. Brazilian Journal of Microbiology, 43, 375-381. https://doi.org/10.1590/S1517-838220120001000045
• Murugaiyan, J., Anand Kumar, P., Rao, G.S., Iskandar, K., Hawser, S., Hays, J.P., Mohsen, Y., Adukkadukkam, S., Awuah, W.A., Jose, R.A.M., Sylvia, N., Nansubuga, E.P., Tilocca, B., Roncada, P., Roson-Calero, N., Moreno-Morales, J., Amin, R., Krishna Kumar, B., Kumar, A., Toufik, A.R, Zaw, T.N, Akinwotu, O.O, Satyaseela M.P., van Dongen, M.B.M. (2022). Progress in alternative strategies to combat antimicrobial resistance: focus on antibiotics. Antibiotics, 11(2), 200. https://doi.org/10.3390/antibiotics11020200
• Negri, I., Mavris, C., Di Prisco, G., Caprio, E., & Pellecchia, M. (2015). Honey bees (Apis mellifera, L.) as active samplers of airborne particulate matter. PLoS One, 10, e0132491. https://doi.org/10.1371/journal.pone.0132491
• Ngalimat, M.S., Raja Abd. Rahman, R.N.Z., Yusof, M.T., Syahir, A., & Sabri, S. (2019). Characterisation of bacteria isolated from the stingless bee, Heterotrigona itama, honey, bee bread and propolis. Peer J, 7, e7478. https://doi.org/10.7717/peerj.7478
• Paredes, D.O., Haro, M., Leoro-Garzon, P., Barba, P., Loaiza, K., Mora, F., Fors, M., Vinueza-Burgos, C., & Fernández-Moreira, E. (2019). Multidrug-resistant Escherichia coli isolated from canine feces in a public park in Quito, Ecuador. Journal of Global Antimicrobial Resistance, 18, 263-268. https://doi.org/10.1016/j.jgar.2019.04.002
• Piva, S., Giacometti, F., Marti, E., Massella, E., Cabbri, R., Galuppi, R., & Serraino, A. (2020). Could honey bees signal the spread of antimicrobial resistance in the environment? Letters in Applied Microbiology, 70(5), 349-355. https://doi.org/10.1111/LAM.13288
• Porrini, C., Caprio, E., Tesoriero, D., & Prisco, G.D. (2014). Using honey bee as bioindicator of chemicals in Campanian agroecosystems (South Italy). Bulletin Insectology, 67(1), 137-146.
• Porrini, C., Ghini, S., Girotti, S., Sabatini, A.G., Gattavecchia, E., & Celli, G. (2002). Use of honey bees as bioindicators of environmental pollution in Italy. In: Devillers, J. & Pham-Delegue, M. (Eds.), Honey Bees: Estimating the Environmental Impact of Chemicals (pp. 186-247). Taylor & Francis.
• Resci, I., & Cilia, G. (2023). The use of honey bee (Apis mellifera L.) as biological monitors for pathogenic bacteria and antimicrobial resistance: A systematic review. Environmental Pollution, 333, 122120. https://doi.org/10.1016/j.envpol.2023.122120
• Rizvi, S.G., & Ahammad, S.Z. (2022). COVID-19 and antimicrobial resistance: a cross-study. Science of The Total Environment, 807, 150873. https://doi.org/10.1016/J.SCITOTENV.2021.150873
• Santaniello, A., Sansone, M., Fioretti, A., Menna, L.F. (2020). Systematic review and meta-analysis of the occurrence of ESKAPE bacteria group in dogs, and the related zoonotic risk in animalassisted therapy, and in animal-assisted activity in the health context. International Journal of Environmental Research and Public Health, 17(9), 3278. https://doi.org/10.3390/ijerph17093278
• Seeley, T.D. (1995). The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies. Harvard University Press.
• Tan, T.Y., Ng, L.S.Y., He, J., Koh, T.H., & Hsu, L.Y. (2009). Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. Antimicrobial Agents and Chemotherapy, 53, 146-149. https://doi.org/10.1128/aac.00862-08
• Tian, B., Fadhil, N.H., Powell, J.E., Kwong, W.K., & Moran, N.A. (2012). Long-term exposure to antibiotics has caused the accumulation of resistance determinants in the gut microbiota of honeybees. mBio, 3(6), e00377-12. https://doi.org/10.1128/MBIO.00377-12
• Tikofsky, L.L., Barlow, J.W., Santisteban, C., & Schukken, Y.H. (2003). A comparison of antimicrobial susceptibility patterns for Staphylococcus aureus in organic and conventional dairy herds. Microbial Drug Resistance, 9(1), 39-45. https://doi.org/10.1089/107662903322541883
• van der Steen, J.J.M., Cornelissen, B., Blacqui`ere, T., Pijnenburg, J.E.M.L., & Severijnen, M. (2016). Think regionally, act locally: metals in honeybee workers in The Netherlands (surveillance study 2008). Environmental Monitoring Assessment, 1888(188), 1-9. https://doi.org/10.1007/S10661-016-5451-8
• Zaghloul, A., Saber, M., Gadow, S., & Awad, F. (2020). Biological indicators for pollution detection in terrestrial and aquatic ecosystems. Bulletin of the National Research Centre, 441(44), 1-11. https://doi.org/10.1186/S42269-020-00385-X
• Zaghloul, H.A.H., & El Halfawy, N.M. (2022). Genomic insights into antibiotic-resistance and virulence genes of Enterococcus faecium strains from the gut of Apis mellifera. Microbial Genomics, 8(11), mgen000896. https://doi.org/10.1099/MGEN.0.000896
• Zogg, A.L., Zurfluh, K., Schmitt, S., Nüesch-Inderbinen, M., & Stephan, R. (2018). Antimicrobial resistance, multilocus sequence types, and virulence profiles of ESBL producing and non-ESBL producing uropathogenic Escherichia coli isolated from cats and dogs in Switzerland. Veterinary Microbiology, 216, 79-84. https://doi.org/10.1016/j.vetmic.2018.02.011
• Zurek, L., & Ghosh, A. (2014). Insects represent a link between food animal farms and the urban environment for antibiotic resistance traits. Applied Environmental Microbiology, 80(12), 3562-3567. https://doi.org/10.1128/AEM.00600-14