Sulfonamide resistance genes in soils treated with waste from animal production in an organic production system
DOI:
https://doi.org/10.5433/1679-0359.2021v42n3Supl1p2031Keywords:
Animal waste, Antimicrobial resistance, Bovine manure, Poultry litter.Abstract
Animal waste is widely used in organic production systems. However, these residues can increase antimicrobial determinants in the soil. In this perspective, this study was developed to evaluate the presence of sulfonamide resistance genes in soils from an organic production system that received animal waste as organic fertilizer. Soil samples were collected from four properties with different management practices to increase soil fertility. Three properties use the animal waste from the conventional system and the other use plant residues as soil cover and a legal reserve. The extraction of total DNA from soil was carried out followed by the amplification of genes encoding sulfonamide resistance (sul1 and sul2) by the PCR (polymerase chain reaction) technique. The sul1 and sul2 genes were detected only in soils treated with animal waste. The genes were not detected in soils from the legal reserve and the property that used plant residues as soil cover. These results indicate that the use of animal waste as agricultural fertilizer can increase genes for resistance to antimicrobials in the soil and the composting process may not be enough to eliminate them. This information reiterates the need to implement standards that establish quality parameters for animal waste, considering resistance to antimicrobials, as well as the development of management strategies that reduce the risk of spreading resistance to antimicrobials when these residues are applied to soils.Downloads
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References
Amann, R. I., Ludwig, W., & Schleifer, K. H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiology and Molecular Biology Reviews, 59(1), 143-169. doi: 10.1128/mmbr.59.1.143-169.1995
Barbosa, M. P., F., Silva, O. F.(1994). Aspectos agro-econômicos da calagem e da adubação nas culturas de arroz e feijão irrigados. Pesquisa Agropecuária Brasileira, 29(11), 657-1667.
Blum, L. E. B., Amarante, C. V. T., Güttler, G., Macedo, A. F., Kothe, D. M., Simmler, A. O., Prado, G. & Guimarães, L. S. (2006). Produção de moranga e pepino em solo com incorporação de cama aviária e casca de pinus. Horticultura Brasileira, 21(4), 627-631. doi: 10.1590/S0102-05362003000400010
Cadena, M., Durso, L. M., Miller, D. N., Waldrip, H. M., Castleberry, B. L., Drijber, R. A., & Wortmann, C. (2018). Tetracyclineand sulfonamide antibiotic resistance genes in soils from Nebraska organic farming operations. Frontieres in Microbiology, 9, 1283. doi: 10.3389/fmicb.2018.01283
Caires, E. F., Kusman, M. T., Barth, G., Garbuio, F. J., & Padilha, J. M. (2004). Alterações químicas do solo e resposta do milho à calagem e aplicação de gesso. Revista Brasileira de Ciência do Solo, 28(1), 125-136. doi: 10.1590/S0100-06832004000100013
Donagema, G. K., Campos, D. V. B., Calderano, S. B., Teixeira, W. G., & Viana, J. H. M. (2011). Manual de métodos de análises de solos (2a ed. rev.). (EMBRAPA Solos, Documentos, 132). Rio de Janeiro: EMBRAPA Solos.
Faucon, M., Houben, D., & Lambers, H. (2017). Plant functional traits: soil and ecosystem services. Trends Plant Science, 22(5), 385-394. doi: 10.1016/j.tplants.2017.01.005
Heuer, H., & Smalla, K. (2007). Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environmental Microbiology, 9(3), 657-666. doi: 10.1111/j. 1462-2920.2006.01185.x
Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., & Bredesen, D. E. (1993). Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science, 262(5137), 1274-1277. doi: 10.1126/science.8235659
Kim, K. R., Owens, G., Kwon, S. I., So, K. H., Lee, D. B., & Ok, Y. S. (2011). Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water, Air, & Soil Pollution, 214(1-4), 163-174. doi: 10.1007/s11270-010-0412-2
Instrução Normativa nº 64, de 18 de dezembro de 2008. Aprova o regulamento técnico para os sistemas orgânicos de produção animal e vegetal. Recuperado de http://www.gov.br/agricultura/pt-br/assuntos/ vigilancia-agropecuaria/ivegetal/bebidas-arquivos/in-no-64-de-18-de-dezembro-de-2008.pdf/view
Lei 10.831, de 23 de dezembro de 2003. Dispõe sobre a agricultura orgânica e dá outras providências. Recuperado de http://www.planalto.gov.br/ccivil_03/Leis/2003/L10.831.htm
Lin, H., Sun, W., Zhang, Z., Chapman, S. J., Freitag, T. E., Fu, J., Zhang, X., & Ma, J. (2016). Effects of manure and mineral fertilization strategies on soil antibiotic resistance gene levels and microbial community in a paddy-upland rotation system. Environmental Pollution, 211, 332-337. doi: 10.1016/j. envpol.2016.01.007
Lin, H., Zhang, J., Chen, H., Wang, J., Sun, W., Zhang, X., & Ma, J. (2017). Effect of temperature on sulfonamide antibiotics degradation, and on antibiotic resistance determinants and hosts in animal manures. Science of the Total Environment, 607, 725-732. doi: 10.1016/j.scitotenv.2017.07.057
Maccari, A. P., Segat, J. C., Testa, M., Maluche-Baretta, C. R. D., & Baretta, D. (2020). The effect of composted and non-composted poultry litter on survival and reproduction of folsomia candida. International Jornal of Recycling of Organic West in Agriculture, 9(1), 99-105. doi: 10.30486/ IJROWA.2020.1885804.1012
Orrico, M. A. P. Jr., Orrico, A. C. A., & Lucas, J., Jr. (2009). Compostagem da fração sólida da água residuária de suinocultura. Engenharia Agrícola, 29(3), 483491. doi: 10.1590/S0100-69162009000300 015
Pei, R., Kim, S. C., Carlson, K. H., & Pruden, A. (2006). Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Research, 40(12), 2427-2435. doi: 10.1016/j.watres.2006.04.017
Pimenta, R. L. (2018). Avaliação da resistência antimicrobiana e da virulência em cepas bacterianas isoladas de aves em estabelecimentos de corte e postura no estado do Rio de Janeiro. Tese de doutorado, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brasil.
Qian, X., Sun, W., Gu, J., Wang, X. J., Sun, J. J., Yin, Y. N., & Duan, M. L. (2016). Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. Journal of Hazardous Materials, 315, 61-69. doi: 10.1016/j.jhazmat.2016. 05.002
Ramos, D. P., Castro, A. F., & Camargo, M. N. (1973). Levantamento detalhado de solos da área da Universidade Federal Rural do Rio de Janeiro. Pesquisa Agropecuária Brasileira, 8, 1-27.
Reginato, J. B., & Leal, R. M. P. (2010). Comportamento e impacto ambiental de antibióticos usados na produção animal brasileira. Revista Brasileira de Ciência de Solo, 34(3), 601-616. doi: 10.1590/S0100-06832010000300002
Serafim, V. J., & Ruiz, L. G. P. (2018). Genes bacterianos de resistência no meio ambiente. Revista Científica, 1(1), 1-10. Recuperado de http://189.112.117.16/index.php/revista-cientifica/article/view/103
Sköld, O. (2000). Sulfonamide resistance: mechanisms and trends. Drug Resistance Updates, 3(3), 155-160. doi: 10.1054/drup.2000.0146
Suzuki, M. T., & Giovannoni, S. J. (1996). Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Applied and Environmental Microbiology, 62(2), 625-30. doi: 10. 1128/AEM.62.2.625-630.1996
Thomas, P. Boeckel V., Brower, C., Gilbert, M., Bryan, T., Grenfell, S. A., Levin, Timothy, P. R., Teillant, A., & Laxminarayan, R. (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences, 112 (18), 5649-5654. doi: 10.1073/pnas.1503141112
Wichmann, F., Udikovic-Kolic, N., Andrew, S., & Handelsman, J. (2014). Diverse antibiotic resistance genes in dairy cow manure. MBio, 5(2), e01017-13. doi: 10.1128/mBio.01017-13
Wright, G. D. (2007). The antibiotic resistome: the nexus of chemical and genetic diversity. Nature Reviews Microbiology, 5(3), 175. doi: 10.1038/nrmicro1614
Xie, W. Y., Shen, Q., & Zhao, F. J. (2018). Antibiotics and antibiotic resistance from animalmanures to soil: a review. European Journal of Soil Science, 69(1), 181-195. doi: 10.1111/ejss.12494
Zhu, Y., Johnson, T., Su, J., Qiao, M., Guo, G., Stedtfeld, R., Tiedje, J. M. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences, 110(9), 3435-3440. doi: 10.1073/pnas.1222743110
Barbosa, M. P., F., Silva, O. F.(1994). Aspectos agro-econômicos da calagem e da adubação nas culturas de arroz e feijão irrigados. Pesquisa Agropecuária Brasileira, 29(11), 657-1667.
Blum, L. E. B., Amarante, C. V. T., Güttler, G., Macedo, A. F., Kothe, D. M., Simmler, A. O., Prado, G. & Guimarães, L. S. (2006). Produção de moranga e pepino em solo com incorporação de cama aviária e casca de pinus. Horticultura Brasileira, 21(4), 627-631. doi: 10.1590/S0102-05362003000400010
Cadena, M., Durso, L. M., Miller, D. N., Waldrip, H. M., Castleberry, B. L., Drijber, R. A., & Wortmann, C. (2018). Tetracyclineand sulfonamide antibiotic resistance genes in soils from Nebraska organic farming operations. Frontieres in Microbiology, 9, 1283. doi: 10.3389/fmicb.2018.01283
Caires, E. F., Kusman, M. T., Barth, G., Garbuio, F. J., & Padilha, J. M. (2004). Alterações químicas do solo e resposta do milho à calagem e aplicação de gesso. Revista Brasileira de Ciência do Solo, 28(1), 125-136. doi: 10.1590/S0100-06832004000100013
Donagema, G. K., Campos, D. V. B., Calderano, S. B., Teixeira, W. G., & Viana, J. H. M. (2011). Manual de métodos de análises de solos (2a ed. rev.). (EMBRAPA Solos, Documentos, 132). Rio de Janeiro: EMBRAPA Solos.
Faucon, M., Houben, D., & Lambers, H. (2017). Plant functional traits: soil and ecosystem services. Trends Plant Science, 22(5), 385-394. doi: 10.1016/j.tplants.2017.01.005
Heuer, H., & Smalla, K. (2007). Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environmental Microbiology, 9(3), 657-666. doi: 10.1111/j. 1462-2920.2006.01185.x
Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., & Bredesen, D. E. (1993). Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science, 262(5137), 1274-1277. doi: 10.1126/science.8235659
Kim, K. R., Owens, G., Kwon, S. I., So, K. H., Lee, D. B., & Ok, Y. S. (2011). Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water, Air, & Soil Pollution, 214(1-4), 163-174. doi: 10.1007/s11270-010-0412-2
Instrução Normativa nº 64, de 18 de dezembro de 2008. Aprova o regulamento técnico para os sistemas orgânicos de produção animal e vegetal. Recuperado de http://www.gov.br/agricultura/pt-br/assuntos/ vigilancia-agropecuaria/ivegetal/bebidas-arquivos/in-no-64-de-18-de-dezembro-de-2008.pdf/view
Lei 10.831, de 23 de dezembro de 2003. Dispõe sobre a agricultura orgânica e dá outras providências. Recuperado de http://www.planalto.gov.br/ccivil_03/Leis/2003/L10.831.htm
Lin, H., Sun, W., Zhang, Z., Chapman, S. J., Freitag, T. E., Fu, J., Zhang, X., & Ma, J. (2016). Effects of manure and mineral fertilization strategies on soil antibiotic resistance gene levels and microbial community in a paddy-upland rotation system. Environmental Pollution, 211, 332-337. doi: 10.1016/j. envpol.2016.01.007
Lin, H., Zhang, J., Chen, H., Wang, J., Sun, W., Zhang, X., & Ma, J. (2017). Effect of temperature on sulfonamide antibiotics degradation, and on antibiotic resistance determinants and hosts in animal manures. Science of the Total Environment, 607, 725-732. doi: 10.1016/j.scitotenv.2017.07.057
Maccari, A. P., Segat, J. C., Testa, M., Maluche-Baretta, C. R. D., & Baretta, D. (2020). The effect of composted and non-composted poultry litter on survival and reproduction of folsomia candida. International Jornal of Recycling of Organic West in Agriculture, 9(1), 99-105. doi: 10.30486/ IJROWA.2020.1885804.1012
Orrico, M. A. P. Jr., Orrico, A. C. A., & Lucas, J., Jr. (2009). Compostagem da fração sólida da água residuária de suinocultura. Engenharia Agrícola, 29(3), 483491. doi: 10.1590/S0100-69162009000300 015
Pei, R., Kim, S. C., Carlson, K. H., & Pruden, A. (2006). Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Research, 40(12), 2427-2435. doi: 10.1016/j.watres.2006.04.017
Pimenta, R. L. (2018). Avaliação da resistência antimicrobiana e da virulência em cepas bacterianas isoladas de aves em estabelecimentos de corte e postura no estado do Rio de Janeiro. Tese de doutorado, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brasil.
Qian, X., Sun, W., Gu, J., Wang, X. J., Sun, J. J., Yin, Y. N., & Duan, M. L. (2016). Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. Journal of Hazardous Materials, 315, 61-69. doi: 10.1016/j.jhazmat.2016. 05.002
Ramos, D. P., Castro, A. F., & Camargo, M. N. (1973). Levantamento detalhado de solos da área da Universidade Federal Rural do Rio de Janeiro. Pesquisa Agropecuária Brasileira, 8, 1-27.
Reginato, J. B., & Leal, R. M. P. (2010). Comportamento e impacto ambiental de antibióticos usados na produção animal brasileira. Revista Brasileira de Ciência de Solo, 34(3), 601-616. doi: 10.1590/S0100-06832010000300002
Serafim, V. J., & Ruiz, L. G. P. (2018). Genes bacterianos de resistência no meio ambiente. Revista Científica, 1(1), 1-10. Recuperado de http://189.112.117.16/index.php/revista-cientifica/article/view/103
Sköld, O. (2000). Sulfonamide resistance: mechanisms and trends. Drug Resistance Updates, 3(3), 155-160. doi: 10.1054/drup.2000.0146
Suzuki, M. T., & Giovannoni, S. J. (1996). Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Applied and Environmental Microbiology, 62(2), 625-30. doi: 10. 1128/AEM.62.2.625-630.1996
Thomas, P. Boeckel V., Brower, C., Gilbert, M., Bryan, T., Grenfell, S. A., Levin, Timothy, P. R., Teillant, A., & Laxminarayan, R. (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences, 112 (18), 5649-5654. doi: 10.1073/pnas.1503141112
Wichmann, F., Udikovic-Kolic, N., Andrew, S., & Handelsman, J. (2014). Diverse antibiotic resistance genes in dairy cow manure. MBio, 5(2), e01017-13. doi: 10.1128/mBio.01017-13
Wright, G. D. (2007). The antibiotic resistome: the nexus of chemical and genetic diversity. Nature Reviews Microbiology, 5(3), 175. doi: 10.1038/nrmicro1614
Xie, W. Y., Shen, Q., & Zhao, F. J. (2018). Antibiotics and antibiotic resistance from animalmanures to soil: a review. European Journal of Soil Science, 69(1), 181-195. doi: 10.1111/ejss.12494
Zhu, Y., Johnson, T., Su, J., Qiao, M., Guo, G., Stedtfeld, R., Tiedje, J. M. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences, 110(9), 3435-3440. doi: 10.1073/pnas.1222743110
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2021-04-22
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Oliveira, C. C. de, Bertholoto, D. M., Nascimento, E. C. do, Zonta, E., Coelho, S. de M. de O., Souza, M. M. S. de, … Coelho, I. da S. (2021). Sulfonamide resistance genes in soils treated with waste from animal production in an organic production system. Semina: Ciências Agrárias, 42(3Supl1), 2031–2040. https://doi.org/10.5433/1679-0359.2021v42n3Supl1p2031
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