The ability of Sitophilus oryzae (Coleoptera, Curculionidae) to transmit Mycobacterium bovis: Morphology, cultural biochemical properties of the bacteria
Keywords:
mycobacteria; tuberculosis; histology; PCR; genotyping
Abstract
The problem of tuberculosis has been relevant for many years due to active spread of the infection pathogen around the globe, in particular in Ukraine. In this article, we determined the epizootic role of the rice weevil (Sitophilus oryzae (Linnaeus, 1763); Coleoptera, Curculionidae) in the spread of Mycobacterium bovis. We identified the effect of the beetle on properties of the pathogen, particularly the changes in morphology, cultural, biochemical, and biological properties after the bacteria had travelled through the body of the rice weevil. To achieve our objectives, we used the museum 100th passage of the virulent strain of M. bovis. We employed microscopic, cultural, biochemical, biological (infecting the biological model), pathoanatomic, histological methods, and PCR studies. The rice weevil is able to retain mycobacteria and release them into their environment for 30 days after becoming infected, with gradual decrease in the number of microbial cells. According to morphology and cultural properties, the pathogen we isolated in the experiment was identical to the initial culture. Enzymatic activity of the bacteria varied. The bacteria that had passed through the intestines of M. bovis were observed to have changes in the biochemical parameters which helped them to adapt to the new environment. We measured the effect of the rice weevil on pathogenicity of M. bovis, isolated directly from the beetle and from grain contaminated with the insects during the experiment. The practical importance of the study consists in expansion of our understanding of the ways M. bovis spreads, identification of effect the rice weevil has on mycobacteria. It also might help in the search for ways to interrupt the chain of tuberculosis transmission – prevention of spread of the disease to favourable areas.References
Bañuls, A. L., Sanou, A., Van Anh, N. T., & Godreuil, S. (2015). Mycobacterium tuberculosis: Ecology and evolution of a human bacterium. Journal of Medical Microbiology, 64(11), 1261–1269.
Cano, J., Rodríguez, A., Simpson, H., Tabah, E. N., Gomez, J. F., & Pullan, R. L. (2018). Modelling the spatial distribution of aquatic insects (order Hemiptera) potentially involved in the transmission of Mycobacterium ulcerans in Africa. Parasites Vectors, 11, 501.
Crispell, J., Benton, C. H., Balaz, D., De Maio, N., Ahkmetova, A., Allen, A., Biek, R., Presho, E. L., Dale, J., Hewinson, G., Lycett, S. J., Nunez-Garcia, J., Skuce, R. A., Trewby, H., Wilson, D. J., Zadoks, R. N., Delahay, R. J., & Kao, R. R. (2019). Combining genomics and epidemiology to analyse bi-directional transmission of Mycobacterium bovis in a multi-host system. eLife, 8, e45833.
Fischer, O. A., Matlova, L., Dvorska, L., Svastova, P., Bartl, J., Weston, R. T., & Pavlik, I. (2004). Blowflies Calliphora vicina and Lucilia sericata as passive vectors of Mycobacterium avium subsp. avium, M. a. paratuberculosis and M. a. hominissuis. Medical and Veterinary Entomology, 18(2), 116–122.
Fritz, C. (2002). Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infection and Immunity, 70(1), 286–291.
Gao, J., Guo, M., Teng, L., Bao, R., Xian, Q., Wang, X., & Ho, W. (2018). Guinea pig infected with Mycobacterium tuberculosis via oral consumption. Journal of Applied Animal Research, 46(1), 1323–1328.
Gotsulya, А. S., Zazharskyі, V. V., Davidenko, P. O., Zazharska, N. M., Kulishenko, O. M., Panasenko, O. I., Gutyj, B. V., Pryima, O. B., Mazur, I. Y., Pritsak, V. V., Drachuk, U. R., Sobolta, A. G., & Riy, M. B. (2020). Features of experimental modeling of tuberculosis in guinea pig with the participation of N'-(2-(5- ((thephylline-7'-yl)methyl)-4-R-1,2,4-triazole-3-ylthio)acethyl)isonicotinohydrazide. Ukrainian Journal of Ecology, 10(4), 191–194.
Hauer, A., Michelet, L., De Cruz, K., Cochard, T., Branger, M., Karoui, C., Henault, S., Biet, F., & Boschiroli, M. L. (2016). MIRU-VNTR allelic variability depends on Mycobacterium bovis clonal group identity. Infection, Genetics and Evolution, 45, 165–169.
Hayashi, D., Takii, T., Mukai, T., Makino, M., Yasuda, E., Horita, Y., Yamamoto, R., Fujiwara, A., Kanai, K., Kondo, M., Kawarazaki, A., Yano, I., Yamamoto, S., & Onozaki, K. (2010). Biochemical characteristics among Mycobacterium bovis BCG substrains. FEMS Microbiology Letters, 306(2), 103–109.
Horalskyi, L. P., Khomych, V. T., & Kononskyi, O. I. (2005). Osnovy histolohichnoji tekhniky i morfofunktsyonalni metody doslidzhen’ u normi ta pry patolohiji [Fundamentals of histological technique and morphofunctional methods of research in norm and at pathology]. Polissia, Zhytomyr (in Ukrainian).
Kam, K. M., Yip, C. W., Tse, L. W., Leung, K. L., Wong, K. L., Ko, W. M., & Wong, W. S. (2006). Optimization of variable number tandem repeat typing set for differentiating Mycobacterium tuberculosis strains in the Beijing family: Optimized VNTR typing of M. tuberculosis Beijing family. FEMS Microbiology Letters, 256(2), 258–265.
Kazda, J. (2000). The ecology of mycobacteria. Springer, Dordrecht.
Marsollier, L., Robert, R., Aubry, J., Saint André, J. P., Kouakou, H., Legras, P., Manceau, A. L., Mahaza, C., & Carbonnelle, B. (2002). Aquatic insects as a vector for Mycobacterium ulcerans. Applied and Environmental Microbiology, 68(9), 4623–4628.
Martynov, V. O., Hladkyi, O. Y., Kolombar, T. M., & Brygadyrenko, V. V. (2019). Impact of essential oil from plants on migratory activity of Sitophilus granarius and Tenebrio molitor. Regulatory Mechanisms in Biosystems, 10(4), 359–371.
Palchykov, V. A., Zazharskyi, V. V., Brygadyrenko, V. V., Davydenko, P. O., Kulishenko, O. M., Borovik, I. V., Chumak, V., Kryvaya, A., & Boyko, O. O. (2019). Bactericidal, protistocidal, nematodicidal properties and chemical composition of ethanol extract of Punica granatum peel. Biosystems Diversity, 27(3), 300–306.
Pérez-Morote, R., Pontones-Rosa, C., Gortázar-Schmidt, C., & Muñoz-Cardona, Á. I. (2020). Quantifying the economic impact of bovine tuberculosis on livestock farms in South-Western Spain. Animals, 10(12), 2433.
Portaels, F., Chemlal, K., Elsen, P., Johnson, P. D., Hayman, J. A., Hibble, J., Kirkwood, R., & Meyers, W. M. (2001). Mycobacterium ulcerans in wild animals. Revue Scientifique et Technique, 20(1), 252–264.
Sarwar, M. (2015). Insect vectors involving in mechanical transmission of human pathogens for serious diseases. International Journal of Bioinformatics and Biomedical Engineering, 1(3), 300–306.
Sohaskey, C. (2008). Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. Jouenal of Bacteriology, 190, 2981–2986.
Titov, O., & Brygadyrenko, V. (2021). Influence of synthetic flavorings on the migration activity of Tribolium confusum and Sitophilus granarius. Ekologia (Bratislava), 40(2), 163–177.
Tkachenko, O. A., Kozak, N. I., Bilan, M. V., & Ponomarenko, A. R. (2019). Dependence of biochemical activity of Mycobacterium bovis on passages and cultivation temperature. Theoretical and Applied Veterinary Medicine, 7(2), 84–89.
Tkachenko, O., Alifonova, K., Gavrylina, O., & Knight, A. (2021a). Epizootological significance of rice weevil as a Mycobacterium bovis reservoir. Scientific Horizons, 24(3), 28–37.
Tkachenko, O., Kozak, N., Bilan, M., Hlebeniuk, V., Alekseeva, N., Kovaleva, L., Nedosekov, V., & Galatiuk, O. (2021b). The effect of long-term storage on Mycobacterium bovis. Polish Journal of Microbiology, 70(3), 327–337.
Vázquez-Marrufo, G., Marín-Hernández, D., Zavala-Páramo, M. G., Vázquez-Narvaez, G., Álvarez-Aguilar, C., & Vázquez-Garcidueñas, M. S. (2008). Genetic diversity among Mycobacterium tuberculosis isolates from Mexican patients. Canadian Journal of Microbiology, 54(8), 610–618.
Wallace, J. R., Gordon, M. C., Hartsell, L., Mosi, L., Benbow, M. E., Merritt, R. W., & Small, P. L. (2010). Interaction of Mycobacterium ulcerans with mosquito species: Implications for transmission and trophic relationships. Applied and Environmental Microbiology, 76(18), 6215–6222.
Weber, I., Fritz, C., Ruttkowski, S., Kreft, A., & Bange, F. (2000). Anaerobic nitrate reductase (narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunodeficient mice. Molecular Microbiology, 35(5), 1017–1025.
Zarei, O., Shokoohizadeh, L., Hossainpour, H., & Alikhani, M. Y. (2018). Molecular analysis of Pseudomonas aeruginosa isolated from clinical, environmental and cockroach sources by ERIC-PCR. BMC Research Notes, 11, 668.
Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., Zazharska, N. M., & Brygadyrenko, V. V. (2020). Antibacterial and fungicidal activities of ethanol extracts of 38 species of plants. Biosystems Diversity, 28(3), 281–289.
Zazharskyi, V., Alifonova, K., Bilan, M., Kozak, N., & Kasianenko, O. (2022). Influence of Sitophilus oryzae on biological properties of Mycobacterium bovis. Scientific Horizons, 25(11), 20–30.
Zazharskyi, V., Parchenko, M., Fotina, T., Davydenko, P., Kulishenko, O., Zazharskaya, N., & Borovik, I. (2019). Synthesis, structure, physicochemical properties and antibacterial activity of 1,2,4-triazoles-3-thiols and furan derivatives. Voprosy Khimii i Khimicheskoj Tekhnologii, 6, 74–82.
Cano, J., Rodríguez, A., Simpson, H., Tabah, E. N., Gomez, J. F., & Pullan, R. L. (2018). Modelling the spatial distribution of aquatic insects (order Hemiptera) potentially involved in the transmission of Mycobacterium ulcerans in Africa. Parasites Vectors, 11, 501.
Crispell, J., Benton, C. H., Balaz, D., De Maio, N., Ahkmetova, A., Allen, A., Biek, R., Presho, E. L., Dale, J., Hewinson, G., Lycett, S. J., Nunez-Garcia, J., Skuce, R. A., Trewby, H., Wilson, D. J., Zadoks, R. N., Delahay, R. J., & Kao, R. R. (2019). Combining genomics and epidemiology to analyse bi-directional transmission of Mycobacterium bovis in a multi-host system. eLife, 8, e45833.
Fischer, O. A., Matlova, L., Dvorska, L., Svastova, P., Bartl, J., Weston, R. T., & Pavlik, I. (2004). Blowflies Calliphora vicina and Lucilia sericata as passive vectors of Mycobacterium avium subsp. avium, M. a. paratuberculosis and M. a. hominissuis. Medical and Veterinary Entomology, 18(2), 116–122.
Fritz, C. (2002). Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infection and Immunity, 70(1), 286–291.
Gao, J., Guo, M., Teng, L., Bao, R., Xian, Q., Wang, X., & Ho, W. (2018). Guinea pig infected with Mycobacterium tuberculosis via oral consumption. Journal of Applied Animal Research, 46(1), 1323–1328.
Gotsulya, А. S., Zazharskyі, V. V., Davidenko, P. O., Zazharska, N. M., Kulishenko, O. M., Panasenko, O. I., Gutyj, B. V., Pryima, O. B., Mazur, I. Y., Pritsak, V. V., Drachuk, U. R., Sobolta, A. G., & Riy, M. B. (2020). Features of experimental modeling of tuberculosis in guinea pig with the participation of N'-(2-(5- ((thephylline-7'-yl)methyl)-4-R-1,2,4-triazole-3-ylthio)acethyl)isonicotinohydrazide. Ukrainian Journal of Ecology, 10(4), 191–194.
Hauer, A., Michelet, L., De Cruz, K., Cochard, T., Branger, M., Karoui, C., Henault, S., Biet, F., & Boschiroli, M. L. (2016). MIRU-VNTR allelic variability depends on Mycobacterium bovis clonal group identity. Infection, Genetics and Evolution, 45, 165–169.
Hayashi, D., Takii, T., Mukai, T., Makino, M., Yasuda, E., Horita, Y., Yamamoto, R., Fujiwara, A., Kanai, K., Kondo, M., Kawarazaki, A., Yano, I., Yamamoto, S., & Onozaki, K. (2010). Biochemical characteristics among Mycobacterium bovis BCG substrains. FEMS Microbiology Letters, 306(2), 103–109.
Horalskyi, L. P., Khomych, V. T., & Kononskyi, O. I. (2005). Osnovy histolohichnoji tekhniky i morfofunktsyonalni metody doslidzhen’ u normi ta pry patolohiji [Fundamentals of histological technique and morphofunctional methods of research in norm and at pathology]. Polissia, Zhytomyr (in Ukrainian).
Kam, K. M., Yip, C. W., Tse, L. W., Leung, K. L., Wong, K. L., Ko, W. M., & Wong, W. S. (2006). Optimization of variable number tandem repeat typing set for differentiating Mycobacterium tuberculosis strains in the Beijing family: Optimized VNTR typing of M. tuberculosis Beijing family. FEMS Microbiology Letters, 256(2), 258–265.
Kazda, J. (2000). The ecology of mycobacteria. Springer, Dordrecht.
Marsollier, L., Robert, R., Aubry, J., Saint André, J. P., Kouakou, H., Legras, P., Manceau, A. L., Mahaza, C., & Carbonnelle, B. (2002). Aquatic insects as a vector for Mycobacterium ulcerans. Applied and Environmental Microbiology, 68(9), 4623–4628.
Martynov, V. O., Hladkyi, O. Y., Kolombar, T. M., & Brygadyrenko, V. V. (2019). Impact of essential oil from plants on migratory activity of Sitophilus granarius and Tenebrio molitor. Regulatory Mechanisms in Biosystems, 10(4), 359–371.
Palchykov, V. A., Zazharskyi, V. V., Brygadyrenko, V. V., Davydenko, P. O., Kulishenko, O. M., Borovik, I. V., Chumak, V., Kryvaya, A., & Boyko, O. O. (2019). Bactericidal, protistocidal, nematodicidal properties and chemical composition of ethanol extract of Punica granatum peel. Biosystems Diversity, 27(3), 300–306.
Pérez-Morote, R., Pontones-Rosa, C., Gortázar-Schmidt, C., & Muñoz-Cardona, Á. I. (2020). Quantifying the economic impact of bovine tuberculosis on livestock farms in South-Western Spain. Animals, 10(12), 2433.
Portaels, F., Chemlal, K., Elsen, P., Johnson, P. D., Hayman, J. A., Hibble, J., Kirkwood, R., & Meyers, W. M. (2001). Mycobacterium ulcerans in wild animals. Revue Scientifique et Technique, 20(1), 252–264.
Sarwar, M. (2015). Insect vectors involving in mechanical transmission of human pathogens for serious diseases. International Journal of Bioinformatics and Biomedical Engineering, 1(3), 300–306.
Sohaskey, C. (2008). Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. Jouenal of Bacteriology, 190, 2981–2986.
Titov, O., & Brygadyrenko, V. (2021). Influence of synthetic flavorings on the migration activity of Tribolium confusum and Sitophilus granarius. Ekologia (Bratislava), 40(2), 163–177.
Tkachenko, O. A., Kozak, N. I., Bilan, M. V., & Ponomarenko, A. R. (2019). Dependence of biochemical activity of Mycobacterium bovis on passages and cultivation temperature. Theoretical and Applied Veterinary Medicine, 7(2), 84–89.
Tkachenko, O., Alifonova, K., Gavrylina, O., & Knight, A. (2021a). Epizootological significance of rice weevil as a Mycobacterium bovis reservoir. Scientific Horizons, 24(3), 28–37.
Tkachenko, O., Kozak, N., Bilan, M., Hlebeniuk, V., Alekseeva, N., Kovaleva, L., Nedosekov, V., & Galatiuk, O. (2021b). The effect of long-term storage on Mycobacterium bovis. Polish Journal of Microbiology, 70(3), 327–337.
Vázquez-Marrufo, G., Marín-Hernández, D., Zavala-Páramo, M. G., Vázquez-Narvaez, G., Álvarez-Aguilar, C., & Vázquez-Garcidueñas, M. S. (2008). Genetic diversity among Mycobacterium tuberculosis isolates from Mexican patients. Canadian Journal of Microbiology, 54(8), 610–618.
Wallace, J. R., Gordon, M. C., Hartsell, L., Mosi, L., Benbow, M. E., Merritt, R. W., & Small, P. L. (2010). Interaction of Mycobacterium ulcerans with mosquito species: Implications for transmission and trophic relationships. Applied and Environmental Microbiology, 76(18), 6215–6222.
Weber, I., Fritz, C., Ruttkowski, S., Kreft, A., & Bange, F. (2000). Anaerobic nitrate reductase (narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunodeficient mice. Molecular Microbiology, 35(5), 1017–1025.
Zarei, O., Shokoohizadeh, L., Hossainpour, H., & Alikhani, M. Y. (2018). Molecular analysis of Pseudomonas aeruginosa isolated from clinical, environmental and cockroach sources by ERIC-PCR. BMC Research Notes, 11, 668.
Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., Zazharska, N. M., & Brygadyrenko, V. V. (2020). Antibacterial and fungicidal activities of ethanol extracts of 38 species of plants. Biosystems Diversity, 28(3), 281–289.
Zazharskyi, V., Alifonova, K., Bilan, M., Kozak, N., & Kasianenko, O. (2022). Influence of Sitophilus oryzae on biological properties of Mycobacterium bovis. Scientific Horizons, 25(11), 20–30.
Zazharskyi, V., Parchenko, M., Fotina, T., Davydenko, P., Kulishenko, O., Zazharskaya, N., & Borovik, I. (2019). Synthesis, structure, physicochemical properties and antibacterial activity of 1,2,4-triazoles-3-thiols and furan derivatives. Voprosy Khimii i Khimicheskoj Tekhnologii, 6, 74–82.
Published
2023-08-27
How to Cite
Zazharskyi, V. V., Alifonova, K. V., Brygadyrenko, V. V., Zazharska, N. M., Goncharenko, V. P., & Solomon, V. V. (2023). The ability of Sitophilus oryzae (Coleoptera, Curculionidae) to transmit Mycobacterium bovis: Morphology, cultural biochemical properties of the bacteria . Regulatory Mechanisms in Biosystems, 14(3), 476-486. https://doi.org/10.15421/10.15421/022368
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