Soil Bacterial Community Tolerance to Three Tetracycline Antibiotics Induced by Ni and Zn
- Vanesa Santás-Miguel 1
- Laura Rodríguez-González 1
- Avelino Núñez-Delgado 2
- Esperanza Álvarez-Rodríguez 2
- Montserrat Díaz-Raviña 3
- Manuel Arias Estévez 1
- David Fernández Calviño 1
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1
Universidade de Vigo
info
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2
Universidade de Santiago de Compostela
info
- 3 Departamento de Bioquímica del Suelo Misión Biológica de Galicia
ISSN: 2253-6574
Ano de publicación: 2023
Volume: 13
Número: 1
Tipo: Artigo
Outras publicacións en: Spanish Journal of Soil Science: SJSS
Resumo
A laboratory work has been carried out to determine the tolerance of soil bacterial communities to Ni and Zn and co-tolerance to tetracycline antibiotics chlortetracycline (CTC), oxytetracycline (OTC) and tetracycline (TC)) in soils individually spiked with five different concentrations of Ni or Zn (1,000, 750, 500, 250, and 125 mg kg−1 ), and an uncontaminated (0 mg kg−1 ) control soil. The PICT parameter (pollution-induced community tolerance) was estimated for the bacterial community using the tritium (3 H)- labeled leucine incorporation technique, and the values corresponding to log IC50 were used as toxicity index. The mean log IC50 values observed in the uncontaminated soil samples indicate that Zn (with log IC50 = −2.83) was more toxic than Ni (log IC50 = −2.73). In addition, for the soil with the lowest carbon content (C = 1.9%), Ni-contaminated samples showed increased tolerance when the Ni concentrations added were ≥500 mg kg−1 , while for the soils with higher carbon content (between 5.3% and 10.9%) tolerance increased when Ni concentrations added were ≥1,000 mg kg−1 . Regarding the soils contaminated with Zn, tolerance increased in all the soils studied when the Zn concentrations added were ≥125 mg kg−1 , regardless of the soil carbon content. The co-tolerance increases obtained after exposure of the bacterial suspension to TC, OTC and CTC showed an identical behavior within these tetracycline antibiotics. However, it was dependent on the heavy metal tested (Ni or Zn). In the case of soils 1 (C = 1.1%) and 2 (C = 5.3%), the soil bacterial communities showed increases in co-tolerance to TC, OTC and CTC for Ni concentrations added of ≥125 mg kg−1 , while for soil 3 (with C = 10.9%) co-tolerance took place when Ni was added at ≥1,000 mg kg−1 . However, in soils contaminated with Zn, increases in co-tolerance to CTC, OTC and TC occurred at Zn concentrations added of ≥125 mg kg−1 for the 3 soils tested. These results can be considered relevant when anticipating possible environmental repercussions related to the simultaneous presence of various types of pollutants, specifically certain heavy metals and antibiotics.
Información de financiamento
Financiadores
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Ministerio de Economía y Competitividad
- CGL 2015-67333-C2-1-R
- Xunta de Galicia
Referencias bibliográficas
- Abdu, N., Abdullahi, A. A., and Abdulkadir, A. (2017). Heavy Metals and Soil Microbes. Environ. Chem. Lett. 15 (1), 65–84. doi:10.1007/s10311-016-0587-x
- Almås, Å. R., Bakken, L. R., and Mulder, J. (2004). Changes in Tolerance of Soil Microbial Communities in Zn and Cd Contaminated Soils. Soil Biol. biochem. 36 (5), 805–813. doi:10.1016/j.soilbio.2004.01.010
- Bååth, E. (1989). Effects of Heavy Metals in Soil on Microbial Processes and Populations (A Review). Water Air Soil Pollut. 47 (3), 335–379. doi:10.1007/BF00279331
- Berg, J., Thorsen, M. K., Holm, P. E., Jensen, J., Nybroe, O., and Brandt, K. K. (2010). Cu Exposure under Field Conditions Coselects for Antibiotic Resistance as Determined by a Novel Cultivationindependent Bacterial Community Tolerance Assay. Environ. Sci. Technol. 44, 8724–8728. doi:10.1021/es101798r
- Blanck, H. (2002). A Critical Review of Procedures and Approaches Used for Assessing Pollution-Induced Community Tolerance (PICT) in Biotic Communities. Hum. Ecol. Risk Assess. 8 (5), 1003–1034. doi:10.1080/1080-700291905792
- Brookes, P. C. (1995). The Use of Microbial Parameters in Monitoring Soil Pollution by Heavy Metals. Biol. Fertil. Soils. 19 (4), 269–279. doi:10.1007/BF00336094
- Caban, J. R., Kuppusamy, S., Kim, J. H., Yoon, Y. E., Kim, S. Y., and Lee, Y. B. (2018). Green Manure Amendment Enhances Microbial Activity and Diversity in Antibiotic Contaminated Soil. Appl. Soil Ecol. 129, 72–76. doi:10.1016/j.apsoil.2018.04.013
- Chen, J., Li, J., Zhang, H., Shi, W., and Liu, Y. (2019). Bacterial Heavy-Metal and Antibiotic Resistance Genes in a Copper Tailing Dam Area in Northern China. Front. Microbiol. 10, 1916. doi:10.3389/fmicb.2019.01916
- Conde-Cid, M., Álvarez-Esmorís, C., Paradelo-Núñez, R., Nóvoa-Muñoz, J. C., Arias- Estévez, M., Álvarez-Rodríguez, E., et al. (2018). Occurrence of Tetracyclines and Sulfonamides in Manures, Agricultural Soils and Crops from Different Areas in Galicia (NW Spain). J. Clean. Prod. 197, 491–500. doi:10.1016/j.jclepro.2018.06.217
- Davies, J. (1994). Inactivation of Antibiotics and the Dissemination of Resistance Genes. Science 264 (5157), 375–382. doi:10.1126/science.8153624
- Davis, M. R., Zhao, F. J., and McGrath, S. P. (2004). Pollution-induced Community Tolerance of Soil Microbes in Response to a Zinc Gradient. Environ. Toxicol. Chem. 23 (11), 2665–2672. doi:10.1897/03-645
- Diaz-Ravina, M., and Baath, E. (1996). Development of Metal Tolerance in Soil Bacterial Communities Exposed to Experimentally Increased Metal Levels. Appl. Environ. Microbiol. 62 (8), 2970–2977. doi:10.1128/aem.62.8.2970-2977.1996
- Díaz-Raviña, M., Bååth, E., and Frostegård, Å. (1994). Multiple Heavy Metal Tolerance of Soil Bacterial Communities and its Measurement by a Thymidine Incorporation Technique. Appl. Environ. Microbiol. 60 (7), 2238–2247. doi:10.1128/aem.60.7.2238-2247.1994
- Dıaz-Ravina, M., and Bååth, E. (2001). Response of Soil Bacterial Communities Pre-exposed to Different Metals and Reinoculated in an Unpolluted Soil. Soil Biol. biochem. 33 (2), 241–248. doi:10.1016/S0038-0717(00)00136-X
- Dickinson, A. W., Power, A., Hansen, M. G., Brandt, K. K., Piliposian, G., Appleby, P., et al. (2019). Heavy Metal Pollution and Co-selection for Antibiotic Resistance: A Microbial Palaeontology Approach. Environ. Int. 132, 105117. doi:10.1016/j.envint.2019.105117
- Duxbury, T., and Bicknell, B. (1983). Metal-tolerant Bacterial Populations from Natural and Metal-Polluted Soils. Soil Biol. biochem. 15 (3), 243–250. doi:10.1016/0038-0717(83)90066-4
- EC (2006). “European Commission Regulation EC 1881/2006. Setting Maximum Levels for Certain Contaminants in Foodstuffs”,” in Official Journal of the European Union EC 1881/2006. (20.12.2006), L364/365-L364/324.
- European Medicines Agency (2016). “European Surveillance of Veterinary Antimicrobial Consumption,” in Sales of Veterinary Antimicrobial Agents in 29 European Countries in 2014. EMA/61769/2016.
- Fernández-Calviño, D., and Bååth, E. (2013). Co-selection for Antibiotic Tolerance in Cu-Polluted Soil Is Detected at Higher Cu-Concentrations Than Increased Cu-Tolerance. Soil Biol. biochem. 57, 953–956. doi:10.1016/j.soilbio.2012.08.017
- Giller, K. E., Witter, E., and McGrath, S. P. (1999). Assessing Risks of Heavy Metal Toxicity in Agricultural Soils: Do Microbes Matter? Hum. Ecol. Risk Assess. 5 (4), 683–689. doi:10.1080/10807039.1999.9657732
- Giller, K. E., Witter, E., and McGrath, S. P. (2009). Heavy Metals and Soil Microbes. Soil Biol. biochem. 41 (10), 2031–2037. doi:10.1016/j.soilbio.2009.04.026
- Giller, K. E., Witter, E., and Mcgrath, S. P. (1998). Toxicity of Heavy Metals to Microorganisms and Microbial Processes in Agricultural Soils: a Review. Soil Biol. biochem. 30 (10-11), 1389–1414. doi:10.1016/S0038-0717(97)00270-8
- Gluskoter, H. J. (1977). Trace Elements in Coal: Occurrence and Distribution. Urbana, IL. Circular no. 499.
- Hamscher, G., Sczesny, S., Höper, H., and Nau, H. (2002). Determination of Persistent Tetracycline Residues in Soil Fertilized with Liquid Manure by High-Performance Liquid Chromatography with Electrospray Ionization Tandem Mass Spectrometry. Anal. Chem. 74 (7), 1509–1518. doi:10.1021/ac015588m
- Hattori, H. (1992). Influence of Heavy Metals on Soil Microbial Activities. Soil Sci. Plant Nutr. 38 (1), 93–100. doi:10.1080/00380768.1992.10416956
- He, Z., Endale, D. M., Schomberg, H. H., and Jenkins, M. B. (2009). Total Phosphorus, Zinc, Copper, and Manganese Concentrations in Cecil Soil through 10 Years of Poultry Litter Application. Soil Sci. 174 (12), 687–695. doi:10.1097/SS.0b013e3181c30821
- Hejna, M., Gottardo, D., Baldi, A., Dell’Orto, V., Cheli, F., Zaninelli, M., et al. (2018). Review: Nutritional Ecology of Heavy Metals. Animal 12 (10), 2156–2170. doi:10.1017/S175173111700355X
- Hu, H. W., Wang, J. T., Li, J., Shi, X. Z., Ma, Y. B., Chen, D., et al. (2017). Long-term Nickel Contamination Increases the Occurrence of Antibiotic Resistance Genes in Agricultural Soils. Environ. Sci. Technol. 51 (2), 790–800. doi:10.1021/acs.est.6b03383
- Ji, X., Shen, Q., Liu, F., Ma, J., Xu, G., Wang, Y., et al. (2012). Antibiotic Resistance Gene Abundances Associated with Antibiotics and Heavy Metals in Animal Manures and Agricultural Soils Adjacent to Feedlots in Shanghai; China. J. Hazard. Mat. 235, 178–185. doi:10.1016/j.jhazmat.2012.07.040
- Kabata-Pendias, A. (2000). Trace Elements in Soils and Plants. Boca Raton, FL: CRC Press.
- Khan, S. U., and Schnitzer, M. (1978). Soil Organic Matter (No. 631.42 SOI).
- Knapp, C. W., Callan, A. C., Aitken, B., Shearn, R., Koenders, A., and Hinwood, A. (2017). Relationship between Antibiotic Resistance Genes and Metals in Residential Soil Samples from Western Australia. Environ. Sci. Pollut. Res. 24 (3), 2484–2494. doi:10.1007/s11356-016-7997-y
- Knapp, C. W., Dolfing, J., Ehlert, P. A., and Graham, D. W. (2010). Evidence of Increasing Antibiotic Resistance Gene Abundances in Archived Soils since 1940. Environ. Sci. Technol. 44 (2), 580–587. doi:10.1021/es901221x
- Knapp, C. W., McCluskey, S. M., Singh, B. K., Campbell, C. D., Hudson, G., and Graham, D. W. (2011). Antibiotic Resistance Gene Abundances Correlate with Metal and Geochemical Conditions in Archived Scottish Soils. PloS One 6 (11), e27300. doi:10.1371/journal.pone.0027300
- Lu, L., Liu, J., Li, Z., Zou, X., Guo, J., Liu, Z., et al. (2020). Antibiotic Resistance Gene Abundances Associated with Heavy Metals and Antibiotics in the Sediments of Changshou Lake in the Three Gorges Reservoir Area, China. Ecol. Indic. 113, 106275. doi:10.1016/j.ecolind.2020.106275
- Macías, F., and Calvo, R. (2008). “Niveles genéricos de referencia de metales pesados y otroselementos traza en suelos de Galicia (Reference values for heavy metals and other traceelements in soils in Galicia),” in Consellería de Medio Ambiente e Desenvolvemento Sostible (Santiago de Compostela, Spain: Xunta de Galicia), 229.
- McBride, M. B. (1994). Environmental Chemistry of Soils. New York: Oxford University Press.
- Meisner, A., Bååth, E., and Rousk, J. (2013). Microbial Growth Responses Upon Rewetting Soil Dried for Four Days or One Year. Soil Biol. Biochem. 66, 188–192. doi:10.1016/j.soilbio.2013.07.014
- Milne, C. J., Kinniburgh, D. G., Van Riemsdijk, W. H., and Tipping, E. (2003). Generic NICA—Donnan Model Parameters for Metal-Ion Binding by Humic Substances. Environ. Sci. Technol. 37 (5), 958–971. doi:10.1021/es0258879
- Nguyen, C. C., Hugie, C. N., Kile, M. L., and Navab-Daneshmand, T. (2019). Association between Heavy Metals and Antibiotic-Resistant Human Pathogens in Environmental Reservoirs: a Review. Front. Environ. Sci. Eng. 13 (3), 46–17. doi:10.1007/s11783-019-1129-0
- Nies, D. H. (1999). Microbial Heavy-Metal Resistance. Appl. Microbiol. Biotechnol. 51 (6), 730–750. doi:10.1007/s002530051457
- Oyetibo, G. O., Ilori, M. O., Adebusoye, S. A., Obayori, O. S., and Amund, O. O. (2010). Bacteria with Dual Resistance to Elevated Concentrations of Heavy Metals and Antibiotics in Nigerian Contaminated Systems. Environ. Monit. Assess. 168 (1), 305–314. doi:10.1007/s10661-009-1114-3
- Pal, C., Bengtsson-Palme, J., Kristiansson, E., and Larsson, D. G. (2015). Co-occurrence of Resistance Genes to Antibiotics, Biocides and Metals Reveals Novel Insights into Their Co-selection Potential. BMC genomics 16 (1), 964–1014. doi:10.1186/s12864-015-2153-5
- Piccolo, A. (1989). Reactivity of Added Humic Substances towards Plant Available Heavy Metals in Soils. Sci. Total Environ. 81, 607–614. doi:10.1016/0048-9697(89)90169-1
- Refaey, Y., Jansen, B., El-Shater, A. H., El-Haddad, A. A., and Kalbitz, K. (2014). The Role of Dissolved Organic Matter in Adsorbing Heavy Metals in Clay-Rich Soils. Vadose Zone J. 13 (7), vzj2014010009. doi:10.2136/vzj2014.01.0009
- Rodríguez-López, L., Santás-Miguel, V., Núñez-Delgado, A., Álvarez-Rodríguez, E., Pérez-Rodríguez, P., and Arias-Estévez, M. (2022). Influence of pH, Humic Acids, and Salts on the Dissipation of Amoxicillin and Azithromycin under Simulated Sunlight. Span. J. Soil Sci. 12. doi:10.3389/sjss.2022.10438
- Rule, J. H. (1999). Trace Metal Cation Adsorption in Soils: Selective Chemical Extractions and Biological Availability. Stud. Surf. Sci. Catal. 120, 319–349. doi:10.1016/S0167-2991(99)80364-4
- Santás-Miguel, V., Arias-Estévez, M., Díaz-Raviña, M., Fernández-Sanjurjo, M. J., Álvarez-Rodríguez, E., Núñez-Delgado, A., et al. (2020b). Bacterial Community Tolerance to Tetracycline Antibiotics in Cu Polluted Soils. Agronomy 10, 1220. doi:10.3390/agronomy10091220
- Santás-Miguel, V., Arias-Estévez, M., Díaz-Raviña, M., Fernández-Sanjurjo, M. J., Álvarez-Rodríguez, E., Núñez-Delgado, A., et al. (2020d). Effect of Oxytetracycline and Chlortetracycline on Bacterial Community Growth in Agricultural Soils. Agronomy 10 (7), 1011. doi:10.3390/agronomy10071011
- Santás-Miguel, V., Arias-Estévez, M., Díaz-Raviña, M., Fernández-Sanjurjo, M. J., Álvarez-Rodríguez, E., Núñez-Delgado, A., et al. (2020c). Interactions between Soil Properties and Tetracycline Toxicity Affecting to Bacterial Community Growth in Agricultural Soil. Appl. Soil Ecol. 147, 103437. doi:10.1016/j.apsoil.2019.103437
- Santás-Miguel, V., Díaz-Raviña, M., Martín, A., García-Campos, E., Barreiro, A., Núñez-Delgado, A., et al. (2020a). Medium-term Influence of Tetracyclines on Total and Specific Microbial Biomass in Cultivated Soils of Galicia (NW Spain). Span. J. Soil Sci. 10, 217–232. doi:10.3232/SJSS.2020.V10.N3.05
- Santás-Miguel, V., Núñez-Delgado, A., Álvarez-Rodríguez, E., Díaz-Raviña, M., Arias-Estévez, M., and Fernández-Calviño, D. (2022). Tolerance of Soil Bacterial Community to Tetracycline Antibiotics Induced by as, Cd, Zn, Cu, Ni, Cr, and Pb Pollution. SOIL 8 (1), 437–449. doi:10.5194/soil-8-437-2022
- Sapkota, A., Sapkota, A. R., Kucharski, M., Burke, J., McKenzie, S., Walker, P., et al. (2008). Aquaculture Practices and Potential Human Health Risks: Current Knowledge and Future Priorities. Environ. Int. 34 (8), 1215–1226. doi:10.1016/j.envint.2008.04.009
- Sarmah, A. K., Meyer, M. T., and Boxall, A. B. (2006). A Global Perspective on the Use, Sales, Exposure Pathways, Occurrence, Fate and Effects of Veterinary Antibiotics (VAs) in the Environment. Chemosphere 65 (5), 725–759. doi:10.1016/j.chemosphere.2006.03.026
- Sauvé, S., Manna, S., Turmel, M. C., Roy, A. G., and Courchesne, F. (2003). Solid− Solution Partitioning of Cd, Cu, Ni, Pb, and Zn in the Organic Horizons of a Forest Soil. Environ. Sci. Technol. 37 (22), 5191–5196. doi:10.1021/es030059g
- Sebaugh, J. L. (2011). Guidelines for Accurate EC50/IC50 Estimation. Pharm. Stat. 10 (2), 128–134. doi:10.1002/pst.426
- Seiler, C., and Berendonk, T. U. (2012). Heavy Metal Driven Co-selection of Antibiotic Resistance in Soil and Water Bodies Impacted by Agriculture and Aquaculture. Front. Microbiol. 3, 399. doi:10.3389/fmicb.2012.00399
- Serwecińska, L. (2020). Antimicrobials and Antibiotic-Resistant Bacteria: a Risk to the Environment and to Public Health. Water 12 (12), 3313. doi:10.3390/w12123313
- Song, J., Rensing, C., Holm, P. E., Virta, M., and Brandt, K. K. (2017). Comparison of Metals and Tetracycline as Selective Agents for Development of Tetracycline Resistant Bacterial Communities in Agricultural Soil. Environ. Sci. Technol. 51 (5), 3040–3047. doi:10.1021/acs.est.6b05342
- Spark, K. M., Wells, J. D., and Johnson, B. B. (1997). The Interaction of a Humic Acid with Heavy Metals. Soil Res. 35 (1), 89–102. doi:10.1071/S96008
- Stefanowicz, A. M., Niklińska, M., and Laskowski, R. (2009). Pollution-induced Tolerance of Soil Bacterial Communities in Meadow and Forest Ecosystems Polluted with Heavy Metals. Eur. J. Soil Biol. 45 (4), 363–369. doi:10.1016/j.ejsobi.2009.05.005
- Swift, M. J. (1994). “Maintaining the Biological Status of Soil: a Key to Sustainable Land Management,” in Soil Resilience and Sustainable Land Use. Editors D. J. Greenland,, and I. Szabolcs (Wallingford: CAB), 33–39.
- Thiele-Bruhn, S. (2005). Microbial Inhibition by Pharmaceutical Antibiotics in Different Soils—Dose-response Relations Determined with the Iron (III) Reduction Test. Environ. Toxicol. Chem. 24 (4), 869–876. doi:10.1897/04-166R.1
- Toth, J. D., Feng, Y., and Dou, Z. (2011). Veterinary Antibiotics at Environmentally Relevant Concentrations Inhibit Soil Iron Reduction and Nitrification. Soil Biol. biochem. 43 (12), 2470–2472. doi:10.1016/j.soilbio.2011.09.004
- Urra, J., Alkorta, I., Lanzén, A., Mijangros, I., and Garbisu, C. (2019). The Application of Fresh and Composted Horse and Chicken Manure Affects Soil Quality, Microbial Composition and Antibiotic Resistance. Appl. Soil Ecol. 135, 73–84. doi:10.1016/j.apsoil.2018.11.005
- Wu, L., Pan, X., Chen, L., Huang, Y., Teng, Y., Luo, Y., et al. (2013). Occurrence and Distribution of Heavy Metals and Tetracyclines in Agricultural Soils after Typical Land Use Change in East China. Environ. Sci. Pollut. Res. 20, 8342–8354. doi:10.1007/s11356-013-1532-1
- Xu, Y., Xu, J., Mao, D., and Luo, Y. (2017). Effect of the Selective Pressure of Sub-lethal Level of Heavy Metals on the Fate and Distribution of ARGs in the Catchment Scale. Environ. Pollut. 220, 900–908. doi:10.1016/j.envpol.2016.10.074
- Zhang, F., Li, Y., Yang, M., and Li, W. (2012). Content of Heavy Metals in Animal Feeds and Manures from Farms of Different Scales in Northeast China. Int. J. Environ. Res. Public Health. 9 (8), 2658–2668. doi:10.3390/ijerph9082658
- Zhong, Q., Cruz-Paredes, C., Zhang, S., and Rousk, J. (2021). Can Heavy Metal Pollution Induce Bacterial Resistance to Heavy Metals and Antibiotics in Soils from an Ancient Land-Mine? J. Hazard. Mat. 411, 124962. doi:10.1016/j.jhazmat.2020.124962