Pheno-genotypic characterization of the enteromicrobiota of wild and zoo animals as a natural reservoir of antibiotic-resistant microbial strains
Abstract
Background. Currently, there is increasing attention to the rise in the number of cases of bacteria with multiple antimicrobial resistance found in the environment, including in wildlife. Wild animals may play a significant role in the transmission of antibiotic resistance on the local and global levels. The genetic determinants of antibiotic resistance originated in environmental microorganisms, thus a thorough analysis of habitats is necessary to predict the processes of evolution and spread of antibiotic resistance.
There is increasing attention of cases of antimicrobial-resistant bacteria being detected in wildlife is attracting increased attention from scientists. Wild animals are involved in the transmission of antibiotic resistance in microorganisms. The genetic determinants of resistance arose in environmental microorganisms, so a thorough analysis of their habitats is necessary to predict the processes of evolution and spread of this phenomenon.
Purpose. The objective of the study is to examine the pheno-genotypic profile of antibiotic resistance in microorganisms isolated from the enteromicrobiota of wild and captive (zoo) animals.
Materials and methods. Microorganisms were identified using bacteriological methods and time-of-flight mass spectrometry. The detection of genetic determinants of antibiotic resistance was performed using PCR.
Results. The studies have shown that the microbiota of the digestive tract of wild and zoo animals is represented by five families: Streptococcaceae, Enterobacteriaceae, Bacillaceae, Staphylococcaceae, and Pseudomonadaceae. A high resistance of certain bacterial species (E. coli, Klebsiella pneumoniae, Enterococcus faecalis, and others) to antimicrobial agents of the biosynthetic penicillin group and β-lactamase inhibitors has been established. Additionally, half of the E. coli isolates were found to carry the blaCTX-M gene, which encodes an extended-spectrum β-lactamase. The blaOXA10 gene, encoding class D β-lactamases, was detected in 15.2% of E. coli cultures.
Conclusion. The analysis of actual data from microbiological and molecular-genetic monitoring can serve as an important and effective assessment of the dissemination of clinically significant antimicrobial-resistant microbiota among wild animals.
Sponsorship information. This work was supported by the Russian Science Foundation grant (Agreement No. 23-26-00118 dated January 13, 2023).
EDN: BRAOCI
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References
Ерещенко, М. И., Денисенко, Т. Е., & Болтунов, А. Н. (2019). Биологические свойства микроорганизмов, выделенных от атлантического моржа. В Актуальные проблемы ветеринарной медицины, зоотехнии и биотехнологии: Сборник трудов, 453-454. EDN: https://elibrary.ru/vcxlox
Землянко, О. М., Рогоза, Т. М., & Журавлева, Г. А. (2018). Механизмы множественной устойчивости бактерий к антибиотикам. Экологическая генетика, 16(3), 4-17. https://doi.org/10.17816/ecogen1634-17 EDN: https://elibrary.ru/ynfkb
Лях, Ю. Г., Гринёк, А. Н., Сухоцкая, Е. А., & Солодкий, М. А. (2019). Значение диагностики, анализ носительства возбудителей бактериальных инфекций у охотничьих водоплавающих птиц Беларуси. В Зоологические чтения - 2019: Сборник статей международной научно-практической конференции, 172-174.
Калашникова, В. А., & Демерчян, А. В. (2018). Антибиотикорезистентность бактерий, выделенных у обезьян при кишечных инфекциях. Ветеринарная клиника, (7), 12-15. EDN: https://elibrary.ru/rkmbvk
Киселева, С. В., & Денисенко, Т. Е. (2017). Индикация антибиотикорезистентности штаммов стафилококков у различных видов домашних и диких животных. В Тезисы докладов 70-й Всероссийской конференции, 81-102. EDN: https://elibrary.ru/ysmkvk
Ларцева, Л. В., & Истелюева, А. А. (2011). Геоэкологические особенности антибиотикорезистентности микрофлоры внутренних водотоков г. Астрахани. Геология, география и глобальная энергия, (3), 180-186. EDN: https://elibrary.ru/nykzkh
Лыков, И. Н., & Битков, М. П. (2022). Антибиотикорезистентность микрофлоры кузнечиков. Международный научно-исследовательский журнал, (11), 11. https://doi.org/10.23670/IRJ.2022.125.107 EDN: https://elibrary.ru/wmdhsm
Обухова, О. В., & Ларцева, Л. В. (2014). Особенности антибиотикорезистентности энтеробактерий в дельте р. Волги. Гигиена и санитария, (3), 21-23. EDN: https://elibrary.ru/sjsxoh
Давидович, Н. В., Кукалевская, Н. Н., Башилова, Е. Н., & Бажукова, Т. А. (2020). Основные принципы эволюции антибиотикорезистентности у бактерий. Клиническая лабораторная диагностика, 65(6), 387-393. https://doi.org/10.18821/0869-2084-2020-65-6-387-393 EDN: https://elibrary.ru/ejuexx
Манжурина, О. А., Скогорева, А. М., Ромашов, Б. В., & Ромашова, Н. Б. (2017). Современные тенденции антибиотикорезистентности микробиоты домашних и диких животных. Вестник Воронежского государственного аграрного университета, (1), 41-45. https://doi.org/10.17238/issn2071-2243.2017.1.41 EDN: https://elibrary.ru/yqunuv
Устойчивость к противомикробным препаратам [Электронный ресурс]. Всемирная организация здравоохранения. URL: https://www.who.int/ru/health-topics/antimicrobial-resistance (дата обращения: 11.06.2024).
Martinez, J. L., Fajardo, A., Garmendia, L., Hernandez, A., Linares, J. F., Martinez-Solano, L., & Sanchez, M. B. (n.d.). A global view of antibiotic resistance. FEMS Microbiol. Rev., 33, 44-65.
Baquero, F., Alvarez-Ortega, C., & Martinez, J. L. (2009). Ecology and evolution of antibiotic resistance. Environ Microbiol Rep, 1(6), 469-476.
Bonnedahl, J., & Järhult, J. D. (2014). Antibiotic resistance in wild birds. Ups J Med Sci, 119(2), 113-116.
Koeck, R., Daniels-Haardt, I., Becker, K., Mellmann, A., Friedrich, A. W., Mevius, D., & Schwarz, S., Jurke, A. (2018). Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin Microbiol Infect, 10, 441-449.
Dolejska, M., & Literak, I. (2019). Wildlife is overlooked in the epidemiology of medically important antibiotic-resistant bacteria. Antimicrob Agents Chemother, 63(8), 142-151.
Guenther, S., Ewers, C., & Wieler, L. H. (2011). Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol, 128-158.
Martínez, J. L. (2012). Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Front Microbiol, 1-3.
Wellington, E. M., Boxall, A. B., Cross, P., Feil, E. J., Gaze, W. H., Hawkey, P. M. et al. (2013). The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis, 13(2), 155-165.
Furness, L. E., Campbell, A., Zhang, L., Gaze, W. H., & McDonald, R. A. (2017). Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res, 3, 1121-1129.
References
Ereschenko, M. I., Denisenko, T. E., & Boltunov, A. N. (2019). Biological properties of microorganisms isolated from Atlantic walrus. In Actual problems of veterinary medicine, animal husbandry and biotechnology: Proceedings (pp. 453-454). EDN: https://elibrary.ru/vcxlox
Zemlyanko, O. M., Rogoza, T. M., & Zhuravleva, G. A. (2018). Mechanisms of multiple antibiotic resistance in bacteria. Ecological Genetics, 16(3), 4-17. https://doi.org/10.17816/ecogen1634-17 EDN: https://elibrary.ru/ynfkb
Lyakh, Yu. G., Grinek, A. N., Sukotskaya, E. A., & Solodkyi, M. A. (2019). Importance of diagnostics, analysis of carriage of bacterial infection pathogens in hunting waterfowl of Belarus. In Zoological readings - 2019: Proceedings of the International Scientific and Practical Conference (pp. 172-174).
Kalashnikova, V. A., & Demerchyan, A. V. (2018). Antibiotic resistance of bacteria isolated from monkeys with intestinal infections. Veterinary Clinic, (7), 12-15. EDN: https://elibrary.ru/rkmbvk
Kiseleva, S. V., & Denisenko, T. E. (2017). Indication of antibiotic resistance of staphylococcus strains in various species of domestic and wild animals. In Abstracts of the 70th All-Russian Conference (pp. 81-102). EDN: https://elibrary.ru/ysmkvk
Lartseva, L. V., & Isteleva, A. A. (2011). Geoecological features of antibiotic resistance of microflora of internal waterways of Astrakhan. Geology, Geography and Global Energy, (3), 180-186. EDN: https://elibrary.ru/nykzkh
Lykov, I. N., & Bitkov, M. P. (2022). Antibiotic resistance of grasshopper microflora. International Research Journal, (11), 11. https://doi.org/10.23670/IRJ.2022.125.107 EDN: https://elibrary.ru/wmdhsm
Obukhova, O. V., & Lartseva, L. V. (2014). Features of antibiotic resistance of enterobacteria in the Volga Delta. Hygiene and Sanitation, (3), 21-23. EDN: https://elibrary.ru/sjsxoh
Davidovich, N. V., Kukalevskaya, N. N., Bashilova, E. N., & Bazhukova, T. A. (2020). Main principles of evolution of antibiotic resistance in bacteria. Clinical Laboratory Diagnostics, 65(6), 387-393. https://doi.org/10.18821/0869-2084-2020-65-6-387-393 EDN: https://elibrary.ru/ejuexx
Manzhurina, O. A., Skogoreva, A. M., Romashov, B. V., & Romashova, N. B. (2017). Current trends in antibiotic resistance of microbiota of domestic and wild animals. Bulletin of Voronezh State Agrarian University, (1), 41-45. https://doi.org/10.17238/issn2071-2243.2017.1.41 EDN: https://elibrary.ru/yqunuv
Antimicrobial resistance. (2024). World Health Organization. Retrieved from https://www.who.int/ru/health-topics/antimicrobial-resistance (Accessed: June 11, 2024)
Martinez, J. L., Fajardo, A., Garmendia, L., Hernandez, A., Linares, J. F., Martinez-Solano, L., & Sanchez, M. B. (n.d.). A global view of antibiotic resistance. FEMS Microbiol. Rev., 33, 44-65.
Baquero, F., Alvarez-Ortega, C., & Martinez, J. L. (2009). Ecology and evolution of antibiotic resistance. Environ Microbiol Rep, 1(6), 469-476.
Bonnedahl, J., & Järhult, J. D. (2014). Antibiotic resistance in wild birds. Ups J Med Sci, 119(2), 113-116.
Koeck, R., Daniels-Haardt, I., Becker, K., Mellmann, A., Friedrich, A. W., Mevius, D., & Schwarz, S., Jurke, A. (2018). Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin Microbiol Infect, 10, 441-449.
Dolejska, M., & Literak, I. (2019). Wildlife is overlooked in the epidemiology of medically important antibiotic-resistant bacteria. Antimicrob Agents Chemother, 63(8), 142-151.
Guenther, S., Ewers, C., & Wieler, L. H. (2011). Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol, 128-158.
Martínez, J. L. (2012). Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Front Microbiol, 1-3.
Wellington, E. M., Boxall, A. B., Cross, P., Feil, E. J., Gaze, W. H., Hawkey, P. M. et al. (2013). The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis, 13(2), 155-165.
Furness, L. E., Campbell, A., Zhang, L., Gaze, W. H., & McDonald, R. A. (2017). Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res, 3, 1121-1129.
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