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Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions

Year 2024, Volume: 17 Issue: 3, 289 - 298, 30.09.2024
https://doi.org/10.30607/kvj.1498693

Abstract

This study aims to reveal the differences that may occur in the susceptibilities of 2 yogurt bacteria strains, S. thermophilus and L. delbrueckii subsp. bulgaricus, to antibiotics under 2 different durations and 3 different stress conditions. The study also introduces new approaches to reduce potential issues in the fermented milk industry containing antibiotics in milk. To this end, the bacteria were exposed to 2 different low-pressure, low-temperature, and magnetic field activities under 2 different durations. The research concluded that as the severity of the applied stress conditions and application period increase, the antibiotic susceptibility of the bacteria decreases, and resistance to certain antibiotics develops (p<0,05). In the conclusion of the 3 different stress applications, it was found that the bacteria had the highest resistance to antibiotics in the magnetic field applications. In these 3 different stress applications, S. thermophilus showed the highest resistance to lincomycin, cephalexin, and streptomycin; L. delbrueckii subsp. bulgaricus developed resistance to streptomycin, erythromycin, and chloramphenicol. Of the 2 yogurt bacteria, L. delbrueckii subsp. bulgaricus developed a resistance to more antibiotics than S. thermophilus after the stress applications; the developed resistance was also more substantial than that of S. thermophilus.

References

  • Akarca, G., Tomar, O., Güney, İ., Erdur, S., & Gök, V. (2019). Determination of sensitivity of some food pathogens to spice extracts. Journal of Food Science and Technology, 56, 5253-5261.
  • Aslım, B., & Beyatlı, Y. (2004). Antibiotic resistance and plas-mid DNA contents of Streptococcus thermophilus strains isolated from Turkish yoghurts. The Journal of Food Science and Technology, 41, 18- 22.
  • Başyiğit, Kılıç., G. (2014). Identification of lactic acid bacteria isolated from different cheese types and investigation of their use in the dairy industry, TAGEM-11/AR-GE/05 (2011-2013), Project Report (unpublished).
  • Butler, R. (2014). Paleomagnetism: Magnetic domains to geologic paleomagnetism : Magnetic domains to geologic terranes. Electronic Edition, University of Portland.
  • Bracquart, P. (1981). An agar medium for the differential enumeration of Streptococcus thermophilus and Lactobacillus bulgaricus in yoghurt. Journal of Applied Bacteriology, 51, 303-305.
  • Brady, M.S. (1988). Antibiotic/antimicrobial residues in milk. Journal of Food Protection, 51(1),8-11.
  • Cecchetto, J., Carvalho, F.C., Santos, A., Fernandes, F.C., & Bueno, P.R. (2015). An impedimetric biosensor for testing pure serum for dengue diagnosis: Sensors and Actuators B. Chemical, 213, 150-154.
  • Chastanet, A., Ferrè, T., & Msadek, T. (2003). Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Molecular Microbiology, 47,1061–1073.
  • Chen, C., Zhao, S., Hao, G., Yu, H., Tian, H., & Zhao, G. (2017). Role of lactic acid bacteria on the yogurt flavour: A review. International Journal of Food Properties, 20,316-330.
  • Chiders, A.B., & Jones, D.H. (1985). Control and prevention of chemical and drug residues ın food animals. Dairy and Food Sanitation, 5(2), 44-46.
  • Dang, W., Wang, S., Tian, S., Chen, B., Sun, F., Li, W., Jiao, Y., & He, L. (2007). Effects of infrasound on activities of 3beta hydroxysteroid dehydrogenase and acid phosphatase of polygonal cells in adrenal cortex zona fasciculate in mice. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi, 25(2),91–95.
  • Devanthi, P.V.P., Linforth, R., Onyeaka, H., & Gkatzionis, K. (2018). Effects of co- inoculation and sequential inoculation of Tetragenococcus halophilus and Zygosaccharomyces rouxii on soy sauce fermentation. Food Chemistry, 240, 1-8. https://doi.org/10.1016/j.foodchem.2017.07.094.
  • Fiocco, D., Collins, M., Muscariello, L., Hols, P., Kleerebezem, M., & Msadek, T., Spano, G. (2009). The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. Journal Bacteriology, 191,1688–1694.
  • Glaasker, E., Heuberger, E.H., Konings, W.N., & Poolman, B. (1998). Mechanism of osmotic activation of the quaternary ammonium compound transporter (QacT) of Lactobacillus plantarum. Journal of Bacteriology, 180, 5540-5546.
  • Jones, G.M., & Seymour, E.H. (1988). Cowside antibiotics resude testing. Journal of Dairy Science, 71, 1691-1699.
  • Koch, S., Oberson, G., Eugster-Meier, E., Meile, L., & Lacroix, C. (2007). Osmotic stress induced by salt increases cell yield, autolytic activity, and survival of lyophilization of Lactobacillus delbrueckii subsp. lactis. International Journal Food Microbiology, 117, 36–42.
  • Kulkarni, A., Siahrostami, S., Patel, A. & Nørskov, J.K. (2018). Understanding catalytic activity trends in the oxygen reduction reaction. Chemical Reviews, 118(5), 2302-2312.
  • Lakhotia, S.C. (2001). Stress biology a paradigm for integrative biology. Biology International The News Magazine of The International Union of Biological Sciences, 40(1-2), 34.
  • Liu, Z., Gao, X., Zhao, J., & Xiang, Y. (2017). The sterilization effect of solenoid magnetic field direction on heterotrophic bacteria in circulating cooling water. Process Engineering, 174, 1296-1302.
  • Molenaar, D., Hagting, A., Alkema, H., Driessen, A. J., & Konings, W.N. (1993). Characteristics and osmoregulatory roles of uptake systems for proline and glycine betaine in Lactococcus lactis. Journal of Bacteriology, 175, 5438-5444.
  • Naruse, Y. (2002). Mechanical vibration model for chromosomes in metaphase of mitosis and possible application to the interruption of cell division. Biosystems, 66, 55–63
  • Özteber M. (2013). Determination of Antibiotic Resistance of Lactic Acid Bacteria Isolated from Fermented Milk Products by Phenotypic and Genotypic Methods. Adnan Menderes University Institute of Science and Technology, Master's Thesis.
  • Papadimitriou, K., Alegría, Á., Bron, P.A., de Angelis, M., Gobbetti, M., Kleerebezem, M., Lemos, J.A., Linares, D. M., Ross, P., Stanton, C., Turroni, F., van Sinderen, D., Varmanen, P., Ventura, M., Zúñiga, M., Tsakalidou, E., & Kok, J. (2016). Stress physiology of lactic acid bacteria. Microbiology and Molecular Biology Reviews, 80(3), 837-90. https://doi.org/10.1128/MMBR.00076-15
  • Pei Zh, Sang H, Li R, Xiao P, He J, Zhuang Zh, Zhu M, Chen J, & Ma H (2006). Infrasound-induced hemodynamics, ultrastructure, and molecular changes in the rat myocardium. Environmental Toxicollogy, 22(2), 169–175.
  • Piuri, M., Sanchez-Rivas, C., & Ruzal, S.M. (2005). Cell wall modifications during osmotic stress in Lactobacillus casei. Journal Applied Microbiology, 98,84–95.
  • Spano, G., & Massa, S. (2006). Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis. Critical Reviews Microbiology, 32,77–86.
  • Shin, Y., Chang, YC, Lee, DS, Berry, J., Sanders, D.W., Ronceray, P., & Brangwynne, C.P. (2018). Liquid nuclear condensates mechanically sense and restructure the genome. Cell, 175(6), 1481-1491.
  • Silver, S. (2003). Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiology Reviews, 27(2-3), 341-353.
  • Song, L., & Aryana, K.J. (2014). Reconstituted yoghurt from yoghurt cultured milk powder mix has better overall characteristics than reconstituted yoghurt from commercial yoghurt powder. Journal of Dairy Science, 97, 6007-6015. https://doi.org/10.3168/jds.2014-8181
  • Tatlı D. (2009). Conventional Milk Determination of Antibiotic Resistance of Lactic Acid Bacteria Isolated from Conventional Dairy Products. Çukurova University Institute of Science and Technology, Master's Thesis.
  • van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S.D., & Maguin, E. (2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, 82,187–216.
  • Wang, K. W., & Hladky, S. B. (1994). Absence of effects of low-frequency, low- 34 amplitude magnetic fields on the properties of gramicidin A channels. Bio-35 Physical Journal, 67, 1473-1483.
  • Wang, B., Long, X., Liu, Y., Duan, C., & Sakanishi, A. (2002). The effects of mechanical vibration on the microstructure of Gerbera jamesonii acrocarpous callus. Colloids Surf B Biointerfaces 23(1), 1–5
  • Wei, W., Zhang, Y. T., Huang, Q. S., & Ni, B. J. (2019). Polyethylene terephthalate microplastics affect hydrogen production from alkaline anaerobic fermentation of waste activated sludge through altering viability and activity of anaerobic microorganisms. Water Research, 163, 114881.
  • Yang, H., He, M., & Wu, C. (2023). Cross protection of lactic acid bacteria during environmental stresses: Stress responses and underlying mechanisms. LWT- Food Science and Technology, 144, 111203. https://doi.org/10.1016/j.lwt.2021.111203
  • Zhang, C., Lu, J., Yang, D., Chen, X., Huang, Y., & Gu, R. (2018). Stress influenced the aerotolerance of Lactobacillus rhamnosus hsryfm 1301. Biotechnology Letters, 40, 729-735. https://doi.org/10.1007/s10529-018-2523-6

Çeşitli Stres Koşullarına Maruz Kalan Yoğurt Bakterilerinin Antibiyotik Direnç Profili

Year 2024, Volume: 17 Issue: 3, 289 - 298, 30.09.2024
https://doi.org/10.30607/kvj.1498693

Abstract

Bu araştırmada iki farklı süre ve üç farklı stres koşulları altında yoğurt bakterileri S. thermophilus ve L. delbrueckii subsp. bulgaricus suşlarının, antibiyotiklere karşı olan duyarlılıklarında meydana gelebilecek değişimlerin belirlenmesi ve fermente süt endüstrisinde antibiyotikli süt kullanımına bağlı ortaya çıkan sorunların azaltılmasında yeni yaklaşımların ortaya konulması amaçlanmıştır. Bu amaçla bakteriler iki farklı sürede olacak şekilde, iki farklı düşük basınç, düşük sıcaklık ve manyetik alan uygulamalarına tabi tutulmuşlardır. Araştırma sonucunda uygulanan stres koşullarının şiddeti ve uygulama zamanı arttıkça bakterilerde oluşan antibiyotik duyarlılığının azaldığı, bazı antibiyotik türlerine karşı ise direnç gelişiminin ortaya çıktığı tespit edilmiştir (p<0,05). Üç farklı stres uygulaması sonucunda bakterilerin antibiyotik türlerine karşı en fazla direnci manyetik alan uygulamalarında oluşturduğu tespit edilmiştir. Üç farklı stres uygulamasında S. thermophilus en fazla linkomisin, sefaleksin ve sitreptomisine, L. delbrueckii subsp. bulgaricus ise, Streptomisin, Erythromycin ve Chloramphenicole karşı direnç geliştirmiştir. İki farklı yoğurt bakterisinden L. delbrueckii subsp. bulgaricus bakterisinin, S. thermophilus’a kıyasla stres uygulamaları sonucunda daha fazla antibiyotiğe karşı direnç geliştirdiği, ayrıca gelişen direncin de S. thermophilus’dan daha yüksek olduğu araştırma sonucunda tespit edilmiştir.

References

  • Akarca, G., Tomar, O., Güney, İ., Erdur, S., & Gök, V. (2019). Determination of sensitivity of some food pathogens to spice extracts. Journal of Food Science and Technology, 56, 5253-5261.
  • Aslım, B., & Beyatlı, Y. (2004). Antibiotic resistance and plas-mid DNA contents of Streptococcus thermophilus strains isolated from Turkish yoghurts. The Journal of Food Science and Technology, 41, 18- 22.
  • Başyiğit, Kılıç., G. (2014). Identification of lactic acid bacteria isolated from different cheese types and investigation of their use in the dairy industry, TAGEM-11/AR-GE/05 (2011-2013), Project Report (unpublished).
  • Butler, R. (2014). Paleomagnetism: Magnetic domains to geologic paleomagnetism : Magnetic domains to geologic terranes. Electronic Edition, University of Portland.
  • Bracquart, P. (1981). An agar medium for the differential enumeration of Streptococcus thermophilus and Lactobacillus bulgaricus in yoghurt. Journal of Applied Bacteriology, 51, 303-305.
  • Brady, M.S. (1988). Antibiotic/antimicrobial residues in milk. Journal of Food Protection, 51(1),8-11.
  • Cecchetto, J., Carvalho, F.C., Santos, A., Fernandes, F.C., & Bueno, P.R. (2015). An impedimetric biosensor for testing pure serum for dengue diagnosis: Sensors and Actuators B. Chemical, 213, 150-154.
  • Chastanet, A., Ferrè, T., & Msadek, T. (2003). Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Molecular Microbiology, 47,1061–1073.
  • Chen, C., Zhao, S., Hao, G., Yu, H., Tian, H., & Zhao, G. (2017). Role of lactic acid bacteria on the yogurt flavour: A review. International Journal of Food Properties, 20,316-330.
  • Chiders, A.B., & Jones, D.H. (1985). Control and prevention of chemical and drug residues ın food animals. Dairy and Food Sanitation, 5(2), 44-46.
  • Dang, W., Wang, S., Tian, S., Chen, B., Sun, F., Li, W., Jiao, Y., & He, L. (2007). Effects of infrasound on activities of 3beta hydroxysteroid dehydrogenase and acid phosphatase of polygonal cells in adrenal cortex zona fasciculate in mice. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi, 25(2),91–95.
  • Devanthi, P.V.P., Linforth, R., Onyeaka, H., & Gkatzionis, K. (2018). Effects of co- inoculation and sequential inoculation of Tetragenococcus halophilus and Zygosaccharomyces rouxii on soy sauce fermentation. Food Chemistry, 240, 1-8. https://doi.org/10.1016/j.foodchem.2017.07.094.
  • Fiocco, D., Collins, M., Muscariello, L., Hols, P., Kleerebezem, M., & Msadek, T., Spano, G. (2009). The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. Journal Bacteriology, 191,1688–1694.
  • Glaasker, E., Heuberger, E.H., Konings, W.N., & Poolman, B. (1998). Mechanism of osmotic activation of the quaternary ammonium compound transporter (QacT) of Lactobacillus plantarum. Journal of Bacteriology, 180, 5540-5546.
  • Jones, G.M., & Seymour, E.H. (1988). Cowside antibiotics resude testing. Journal of Dairy Science, 71, 1691-1699.
  • Koch, S., Oberson, G., Eugster-Meier, E., Meile, L., & Lacroix, C. (2007). Osmotic stress induced by salt increases cell yield, autolytic activity, and survival of lyophilization of Lactobacillus delbrueckii subsp. lactis. International Journal Food Microbiology, 117, 36–42.
  • Kulkarni, A., Siahrostami, S., Patel, A. & Nørskov, J.K. (2018). Understanding catalytic activity trends in the oxygen reduction reaction. Chemical Reviews, 118(5), 2302-2312.
  • Lakhotia, S.C. (2001). Stress biology a paradigm for integrative biology. Biology International The News Magazine of The International Union of Biological Sciences, 40(1-2), 34.
  • Liu, Z., Gao, X., Zhao, J., & Xiang, Y. (2017). The sterilization effect of solenoid magnetic field direction on heterotrophic bacteria in circulating cooling water. Process Engineering, 174, 1296-1302.
  • Molenaar, D., Hagting, A., Alkema, H., Driessen, A. J., & Konings, W.N. (1993). Characteristics and osmoregulatory roles of uptake systems for proline and glycine betaine in Lactococcus lactis. Journal of Bacteriology, 175, 5438-5444.
  • Naruse, Y. (2002). Mechanical vibration model for chromosomes in metaphase of mitosis and possible application to the interruption of cell division. Biosystems, 66, 55–63
  • Özteber M. (2013). Determination of Antibiotic Resistance of Lactic Acid Bacteria Isolated from Fermented Milk Products by Phenotypic and Genotypic Methods. Adnan Menderes University Institute of Science and Technology, Master's Thesis.
  • Papadimitriou, K., Alegría, Á., Bron, P.A., de Angelis, M., Gobbetti, M., Kleerebezem, M., Lemos, J.A., Linares, D. M., Ross, P., Stanton, C., Turroni, F., van Sinderen, D., Varmanen, P., Ventura, M., Zúñiga, M., Tsakalidou, E., & Kok, J. (2016). Stress physiology of lactic acid bacteria. Microbiology and Molecular Biology Reviews, 80(3), 837-90. https://doi.org/10.1128/MMBR.00076-15
  • Pei Zh, Sang H, Li R, Xiao P, He J, Zhuang Zh, Zhu M, Chen J, & Ma H (2006). Infrasound-induced hemodynamics, ultrastructure, and molecular changes in the rat myocardium. Environmental Toxicollogy, 22(2), 169–175.
  • Piuri, M., Sanchez-Rivas, C., & Ruzal, S.M. (2005). Cell wall modifications during osmotic stress in Lactobacillus casei. Journal Applied Microbiology, 98,84–95.
  • Spano, G., & Massa, S. (2006). Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis. Critical Reviews Microbiology, 32,77–86.
  • Shin, Y., Chang, YC, Lee, DS, Berry, J., Sanders, D.W., Ronceray, P., & Brangwynne, C.P. (2018). Liquid nuclear condensates mechanically sense and restructure the genome. Cell, 175(6), 1481-1491.
  • Silver, S. (2003). Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiology Reviews, 27(2-3), 341-353.
  • Song, L., & Aryana, K.J. (2014). Reconstituted yoghurt from yoghurt cultured milk powder mix has better overall characteristics than reconstituted yoghurt from commercial yoghurt powder. Journal of Dairy Science, 97, 6007-6015. https://doi.org/10.3168/jds.2014-8181
  • Tatlı D. (2009). Conventional Milk Determination of Antibiotic Resistance of Lactic Acid Bacteria Isolated from Conventional Dairy Products. Çukurova University Institute of Science and Technology, Master's Thesis.
  • van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S.D., & Maguin, E. (2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, 82,187–216.
  • Wang, K. W., & Hladky, S. B. (1994). Absence of effects of low-frequency, low- 34 amplitude magnetic fields on the properties of gramicidin A channels. Bio-35 Physical Journal, 67, 1473-1483.
  • Wang, B., Long, X., Liu, Y., Duan, C., & Sakanishi, A. (2002). The effects of mechanical vibration on the microstructure of Gerbera jamesonii acrocarpous callus. Colloids Surf B Biointerfaces 23(1), 1–5
  • Wei, W., Zhang, Y. T., Huang, Q. S., & Ni, B. J. (2019). Polyethylene terephthalate microplastics affect hydrogen production from alkaline anaerobic fermentation of waste activated sludge through altering viability and activity of anaerobic microorganisms. Water Research, 163, 114881.
  • Yang, H., He, M., & Wu, C. (2023). Cross protection of lactic acid bacteria during environmental stresses: Stress responses and underlying mechanisms. LWT- Food Science and Technology, 144, 111203. https://doi.org/10.1016/j.lwt.2021.111203
  • Zhang, C., Lu, J., Yang, D., Chen, X., Huang, Y., & Gu, R. (2018). Stress influenced the aerotolerance of Lactobacillus rhamnosus hsryfm 1301. Biotechnology Letters, 40, 729-735. https://doi.org/10.1007/s10529-018-2523-6
There are 36 citations in total.

Details

Primary Language English
Subjects Veterinary Histology and Embryology
Journal Section RESEARCH ARTICLE
Authors

Gökhan Akarca 0000-0002-5055-2722

Ayşe Janseli Denizkara 0000-0002-3078-8914

Early Pub Date September 10, 2024
Publication Date September 30, 2024
Submission Date June 10, 2024
Acceptance Date September 2, 2024
Published in Issue Year 2024 Volume: 17 Issue: 3

Cite

APA Akarca, G., & Denizkara, A. J. (2024). Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions. Kocatepe Veterinary Journal, 17(3), 289-298. https://doi.org/10.30607/kvj.1498693
AMA Akarca G, Denizkara AJ. Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions. kvj. September 2024;17(3):289-298. doi:10.30607/kvj.1498693
Chicago Akarca, Gökhan, and Ayşe Janseli Denizkara. “Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions”. Kocatepe Veterinary Journal 17, no. 3 (September 2024): 289-98. https://doi.org/10.30607/kvj.1498693.
EndNote Akarca G, Denizkara AJ (September 1, 2024) Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions. Kocatepe Veterinary Journal 17 3 289–298.
IEEE G. Akarca and A. J. Denizkara, “Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions”, kvj, vol. 17, no. 3, pp. 289–298, 2024, doi: 10.30607/kvj.1498693.
ISNAD Akarca, Gökhan - Denizkara, Ayşe Janseli. “Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions”. Kocatepe Veterinary Journal 17/3 (September 2024), 289-298. https://doi.org/10.30607/kvj.1498693.
JAMA Akarca G, Denizkara AJ. Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions. kvj. 2024;17:289–298.
MLA Akarca, Gökhan and Ayşe Janseli Denizkara. “Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions”. Kocatepe Veterinary Journal, vol. 17, no. 3, 2024, pp. 289-98, doi:10.30607/kvj.1498693.
Vancouver Akarca G, Denizkara AJ. Antibiotic Resistance Profile of Yogurt Bacteria Exposed to Various Stress Conditions. kvj. 2024;17(3):289-98.

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