Articles | Volume 9, issue 2
https://doi.org/10.5194/soil-9-561-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/soil-9-561-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Increase in bacterial community induced tolerance to Cr in response to soil properties and Cr level in the soil
Claudia Campillo-Cora
CORRESPONDING AUTHOR
Departamento de Bioloxía Vexetal e Ciencia do Solo, Facultade de Ciencias, Universidade de Vigo, As Lagoas s/n, 32004 Ourense, Spain
Instituto de Agroecoloxía e Alimentación (IAA), Universidade de Vigo – Campus Auga, 32004 Ourense, Spain
Daniel Arenas-Lago
Departamento de Bioloxía Vexetal e Ciencia do Solo, Facultade de Ciencias, Universidade de Vigo, As Lagoas s/n, 32004 Ourense, Spain
Instituto de Agroecoloxía e Alimentación (IAA), Universidade de Vigo – Campus Auga, 32004 Ourense, Spain
Manuel Arias-Estévez
Departamento de Bioloxía Vexetal e Ciencia do Solo, Facultade de Ciencias, Universidade de Vigo, As Lagoas s/n, 32004 Ourense, Spain
Instituto de Agroecoloxía e Alimentación (IAA), Universidade de Vigo – Campus Auga, 32004 Ourense, Spain
David Fernández-Calviño
Departamento de Bioloxía Vexetal e Ciencia do Solo, Facultade de Ciencias, Universidade de Vigo, As Lagoas s/n, 32004 Ourense, Spain
Instituto de Agroecoloxía e Alimentación (IAA), Universidade de Vigo – Campus Auga, 32004 Ourense, Spain
Related authors
No articles found.
Vanesa Santás-Miguel, Avelino Núñez-Delgado, Esperanza Álvarez-Rodríguez, Montserrat Díaz-Raviña, Manuel Arias-Estévez, and David Fernández-Calviño
SOIL, 8, 437–449, https://doi.org/10.5194/soil-8-437-2022, https://doi.org/10.5194/soil-8-437-2022, 2022
Short summary
Short summary
A laboratory experiment was carried out for 42 d to study co-selection for tolerance of tetracycline (TC), oxytetracycline (OTC), and chlortetracycline (CTC) in soils polluted with heavy metals (As, Cd, Zn, Cu, Ni, Cr, and Pb). At high metal concentrations, the bacterial communities show tolerance to the metal itself, occurring for all the metals tested in the long term. The bacterial communities of the soil polluted with heavy metals also showed long-term co-tolerance to TC, OTC, and CTC.
Cited articles
Abou Jaoude, L., Castaldi, P., Nassif, N., Pinna, M. V., and Garau, G.: Biochar and compost as gentle remediation options for the recovery of trace elements-contaminated soils, Sci. Total Environ., 711, 134511, https://doi.org/10.1016/j.scitotenv.2019.134511, 2020.
Adriano, D. C.: Trace Elements in Terrestrial Environments, 2 Edn., Springer, New York, https://doi.org/10.1007/978-0-387-21510-5, 2001.
Ao, M., Chen, X., Deng, T., Sun, S., Tang, Y., Morel, J. L., Qiu, R., and Wang, S.: Chromium biogeochemical behaviour in soil-plant systems and remediation strategies: A critical review, J. Hazard. Mater., 424, 127233, https://doi.org/10.1016/j.jhazmat.2021.127233, 2022.
Bååth, E.: Thymidine incorporation into macromolecules of bacteria extracted from soil by homogenization-centrifugation, Soil Biol. Biochem., 24, 1157–1165, https://doi.org/10.1016/0038-0717(92)90066-7, 1992.
Bååth, E.: Thymidine and leucine incorporation in soil bacteria with different cell size, Microb. Ecol., 27, 267–278, https://doi.org/10.1007/BF00182410, 1994.
Bååth, E., Pettersson, M., and Söderberg, K. H.: Adaptation of a rapid and economical microcentrifugation method to measure thymidine and leucine incorporation by soil bacteria, Soil Biol. Biochem., 33, 1571–1574, https://doi.org/10.1016/S0038-0717(01)00073-6, 2001.
Beesley, L., Moreno-Jiménez, E., and Gomez-Eyles, J. L.: Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil, Environ. Pollut., 158, 2282–2287, https://doi.org/10.1016/J.ENVPOL.2010.02.003, 2010.
Bérard, A., Capowiez, L., Mombo, S., Schreck, E., Dumat, C., Deola, F., and Capowiez, Y.: Soil microbial respiration and PICT responses to an industrial and historic lead pollution: a field study, Environ. Sci. Pollut. Res., 23, 4271–4281, https://doi.org/10.1007/s11356-015-5089-z, 2016.
Berg, J., Brandt, K. K., Al-Soud, W. A., Holm, P. E., Hansen, L. H., Sørensen, S. J., and Nybroe, O.: Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term cu exposure, Appl. Environ. Microbiol., 78, 7438–7446, https://doi.org/10.1128/AEM.01071-12, 2012.
Blanck, H.: A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities, Hum. Ecol. Risk Assess., 8, 1003–1034, https://doi.org/10.1080/1080-700291905792, 2002.
Boivin, M. E. Y., Greve, G. D., Kools, S. A. E., van der Wurff, A. W. G., Leeflang, P., Smit, E., Breure, A. M., Rutgers, M., and van Straalen, N. M.: Discriminating between effects of metals and natural variables in terrestrial bacterial communities, Appl. Soil Ecol., 34, 103–113, https://doi.org/10.1016/j.apsoil.2006.03.009, 2006.
Bolan, N. S. and Thiagarajan, S.: Retention and plant availability of chromium in soils as affected by lime and organic matter amendments, Aust. J. Soil Res., 39, 1091–1103, https://doi.org/10.1071/SR00090, 2001.
Bradl, H. B.: Adsorption of heavy metal ions on soils and soils constituents, J. Colloid Interface Sci., 277, 1–18, https://doi.org/10.1016/j.jcis.2004.04.005, 2004.
Campillo-Cora, C., Conde-Cid, M., Arias-Estévez, M., Fernández-Calviño, D., and Alonso-Vega, F.: Specific adsorption of heavy metals in soils: Individual and competitive experiments, Agronomy, 10, 1113, https://doi.org/10.3390/agronomy10081113, 2020.
Campillo-Cora, C., González-Feijoo, R., Arias-Estévez, M., and Fernández-Calviño, D.: Dissolved organic matter as a confounding factor in the determination of pollution-induced community tolerance (PICT) of bacterial communities to heavy metals using the leucine incorporation method, Geoderma, 430, 116335, https://doi.org/10.1016/j.geoderma.2023.116335, 2023
Campillo-Cora, C., Rodríguez-González, L., Arias-Estévez, M., Fernández-Calviño, D., and Soto-Gómez, D.: Influence of physicochemical properties and parent material on chromium fractionation in soils, Processes, 9, 1073, https://doi.org/10.3390/pr9061073, 2021a.
Campillo-Cora, C., Soto-Gómez, D., Arias-Estévez, M., Bååth, E., and Fernández-Calviño, D.: Estimation of baseline levels of bacterial community tolerance to Cr, Ni, Pb, and Zn in unpolluted soils, a background for PICT (pollution-induced community tolerance) determination, Biol. Fertil. Soils, 58, 49–61, https://doi.org/10.1007/s00374-021-01604-x, 2022a.
Campillo-Cora, C., Soto-Gómez, D., Arias-Estévez, M., Bååth, E., and Fernández-Calviño, D.: Bacterial community tolerance to Cu in soils with geochemical baseline concentrations (GBCs) of heavy metals.: Importance for pollution induced community tolerance (PICT) determinations using the leucine incorporation method, Soil Biol. Biochem., 155, 108157, https://doi.org/10.1016/j.soilbio.2021.108157, 2021b.
Campillo-Cora, C., González-Feijoo, R., Arias-Estévez, M., and Fernández-Calviño, D.: Influence of soil properties on the development of bacterial community tolerance to Cu, Ni, Pb and Zn. Environ. Res., 214, 113920, https://doi.org/10.1016/J.ENVRES.2022.113920, 2022b.
Cervantes, C., Campos-García, J., Devars, S., Gutiérrez-Corona, F., Loza-Tavera, H., Torres-Guzmán, J. C., and Moreno-Sánchez, R.: Interactions of chromium with microorganisms and plants, FEMS Microbiol. Rev., 25, 335–347, https://doi.org/10.1016/S0168-6445(01)00057-2, 2001.
Covelo, E. F., Vega, F. A., and Andrade, M. L.: Heavy metal sorption and desorption capacity of soils containing endogenous contaminants, J. Hazard. Mater., 143, 419–430, https://doi.org/10.1016/j.jhazmat.2006.09.047, 2007.
Dias-Ferreira, C., Kirkelund, G. M., and Ottosen, L. M.: Ammonium citrate as enhancement for electrodialytic soil remediation and investigation of soil solution during the process, Chemosphere, 119, 889–895, https://doi.org/10.1016/j.chemosphere.2014.08.064, 2015.
Dotaniya, M. L., Rajendiran, S., Meena, V. D., Saha, J. K., Coumar, M. V., Kundu, S., and Patra, A. K.: Influence of Chromium Contamination on Carbon Mineralization and Enzymatic Activities in Vertisol, Agric. Res., 6, 91–96, https://doi.org/10.1007/S40003-016-0242-6/TABLES/5, 2017.
Fernández-Calviño, D., Arias-Estévez, M., Díaz-Raviña, M., and Bååth, E.: Assessing the effects of Cu and pH on microorganisms in highly acidic vineyard soils, Eur. J. Soil Sci., 63, 571–578, https://doi.org/10.1111/j.1365-2389.2012.01489.x, 2012.
Fernández-Calviño, D., Arias-Estévez, M., Díaz-Raviña, M., and Bååth, E.: Bacterial pollution induced community tolerance (PICT) to Cu and interactions with pH in long-term polluted vineyard soils, Soil Biol. Biochem., 43, 2324–2331, https://doi.org/10.1016/j.soilbio.2011.08.001, 2011.
Fernández-Calviño, D. and Bååth, E.: 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, https://doi.org/10.1016/j.soilbio.2012.08.017, 2013.
Fernández-Calviño, D. and Bååth, E.: Interaction between pH and Cu toxicity on fungal and bacterial performance in soil, Soil Biol. Biochem., 96, 20–29, https://doi.org/10.1016/j.soilbio.2016.01.010, 2016.
Gong, P., Siciliano, S. D., Srivastava, S., Greer, C. W., and Sunahara, G. I.: Assessment of pollution-induced microbial community tolerance to heavy metals in soil using ammonia-oxidizing bacteria and biolog assay, Hum. Ecol. Risk Assess., 8, 1067–1081, https://doi.org/10.1080/1080-700291905828, 2002.
Gonnelli, C. and Renella, G.: Heavy Metals in Soils, 3 Edn., Springer, Dordrecht, Netherlands, https://doi.org/10.1007/978-94-007-4470-7, 2013.
He, Z., Hu, Y., Yin, Z., Hu, Y., and Zhong, H.: Microbial Diversity of Chromium-Contaminated Soils and Characterization of Six Chromium-Removing Bacteria, Environ. Manage., 57, 1319–1328, https://doi.org/10.1007/s00267-016-0675-5, 2016.
Ipsilantis, I. and Coyne, M. S.: Soil microbial community response to hexavalent chromium in planted and unplanted soil, J. Environ. Qual., 36, 638–645, https://doi.org/10.2134/jeq2005.0438, 2007.
Kabata-Pendias, A.: Trace Elements in Soils and Plants, 4 Edn., Boca Raton, CRC Press, Taylor & Francis Group, New York, https://doi.org/10.1201/b10158, 2011.
Kotaś, J. and Stasicka, Z.: Chromium occurrence in the environment and methods of its speciation, Environ. Pollut., 107, 263–283, https://doi.org/10.1016/S0269-7491(99)00168-2, 2000.
Kunito, T., Saeki, K., Oyaizu, H., and Matsumoto, S.: Influences of copper forms on the toxicity to microorganisms in soils, Ecotoxicol. Environ. Saf., 44, 174–181, https://doi.org/10.1006/eesa.1999.1820, 1999.
Lekfeldt, J. D. S., Magid, J., Holm, P. E., Nybroe, O., and Brandt, K. K.: Evaluation of the leucine incorporation technique for detection of pollution-induced community tolerance to copper in a long-term agricultural field trial with urban waste fertilizers, Environ. Pollut., 194, 78–85, https://doi.org/10.1016/j.envpol.2014.07.013, 2014.
Liu, B., Su, G., Yang, Y., Yao, Y., Huang, Y., Hu, L., Zhong, H., and He, Z.: Vertical distribution of microbial communities in chromium-contaminated soil and isolation of Cr(Y)-Reducing strains, Ecotoxicol. Environ. Saf., 180, 242–251, https://doi.org/10.1016/j.ecoenv.2019.05.023, 2019.
Macías-Vázquez, F. and Calvo de Anta, R.: Niveles Genéricos de Referencia de metales pesados y otros elementos traza en suelos de Galicia, Consellería de Medio Ambiente e Desenvolvemento Sostible, Santiago de Compostela, Spain, ISBN 978-84-453-4664-8, 2009.
Meisner, A., Bååth, E., and Rousk, J.: Microbial growth responses upon rewetting soil dried for four days or one year, Soil Biol. Biochem., 66, 188–192, https://doi.org/10.1016/j.soilbio.2013.07.014, 2013.
Mitchell, K., Trakal, L., Sillerova, H., Avelar-González, F. J., Guerrero-Barrera, A. L., Hough, R., and Beesley, L.: Mobility of As, Cr and Cu in a contaminated grassland soil in response to diverse organic amendments; a sequential column leaching experiment, J. Appl. Geochem., 88, 95–102, https://doi.org/10.1016/j.apgeochem.2017.05.020, 2018.
Nannipieri, P., Ascher, J., Ceccherini, M. T., Landi, L., Pietramellara, G., and Renella, G.: Microbial diversity and soil functions, Eur. J. Soil Sci., 54, 655–670, https://doi.org/10.1046/j.1351-0754.2003.0556.x, 2003.
Ogilvie, L. A. and Grant, A.: Linking pollution induced community tolerance (PICT) and microbial community structure in chronically metal polluted estuarine sediments, Mar. Environ. Res., 65, 187–198, https://doi.org/10.1016/j.marenvres.2007.10.002, 2008.
Pradhan, S. K., Kumar, U., Singh, N. R., and Thatoi, H.: Functional diversity and metabolic profile of microbial community of mine soils with different levels of chromium contamination, Int. J. Environ. Health Res., 30, 461–473, https://doi.org/10.1080/09603123.2019.1601686, 2019.
Rousk, J. and Bååth, E.: Growth of saprotrophic fungi and bacteria in soil, FEMS Microbiol. Ecol., 78, 17–30, https://doi.org/10.1111/j.1574-6941.2011.01106.x, 2011.
Santás-Miguel, V., Núñez-Delgado, A., Álvarez-Rodríguez, E., Díaz-Raviña, M., Arias-Estévez, M., and Fernández-Calviño, D.: Tolerance of soil bacterial community to tetracycline antibiotics induced by As, Cd, Zn, Cu, Ni, Cr, and Pb pollution, SOIL, 8, 437–449, https://doi.org/10.5194/soil-8-437-2022, 2022.
Shahid, M., Shamshad, S., Rafiq, M., Khalid, S., Bibi, I., Niazi, N. K., Dumat, C., and Rashid, M. I.: Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: A review, Chemosphere, 178, 513–533, https://doi.org/10.1016/j.chemosphere.2017.03.074, 2017.
Shallari, S., Schwartz, C., Hasko, A., and Morel, J. L.: Heavy metals in soils and plants of serpentine and industrial sites of Albania, Sci. Total Environ., 209, 133–142, https://doi.org/10.1016/S0048-9697(97)00312-4, 1998.
Shi, W., Becker, J., Bischoff, M., Turco, R. F., and Konopka, A. E.: Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination, Appl. Environ. Microbiol., 68, 3859–3866, https://doi.org/10.1128/AEM.68.8.3859-3866, 2002a.
Shi, W., Bischoff, M., Turco, R., and Konopka, A.: Long-term effects of chromium and lead upon the activity of soil microbial communities, Appl. Soil Ecol., 21, 169–177, https://doi.org/10.1016/S0929-1393(02)00062-8, 2002b.
Srinivasa Gowd, S., Ramakrishna Reddy, M., and Govil, P. K.: Assessment of heavy metal contamination in soils at Jajmau (Kanpur) and Unnao industrial areas of the Ganga Plain, Uttar Pradesh, India, J. Hazard. Mater., 174, 113–121, https://doi.org/10.1016/j.jhazmat.2009.09.024, 2010.
Tlili, A., Berard, A., Blanck, H., Bouchez, A., Cássio, F., Eriksson, K. M., Morin, S., Montuelle, B., Navarro, E., Pascoal, C., Pesce, S., Schmitt-Jansen, M., and Behra, R.: Pollution-induced community tolerance (PICT): towards an ecologically relevant risk assessment of chemicals in aquatic systems, Freshw. Biol., 61, 2141–2151, https://doi.org/10.1111/fwb.12558, 2016.
Van Beelen, P., Wouterse, M., Posthuma, L., and Rutgers, M.: Location-specific ecotoxicological risk assessment of metal-polluted soils, Environ. Toxicol. Chem., 23, 2769–2779, https://doi.org/10.1897/03-568, 2004.
Wei, B. and Yang, L.: A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China, Microchem. J., 94, 99–107, https://doi.org/10.1016/j.microc.2009.09.014, 2010.
Wittbrodt, P. R. and Palmer, C. D.: Reduction of Cr(VI) by soil humic acids, Europ. J. Soil Sci., 48, 151–162, https://doi.org/10.1111/j.1365-2389.1997.tb00194.x, 1997.
Yang, Z., Zhang, X., Jiang, Z., Li, Q., Huang, P., Zheng, C., Liao, Q., and Yang, W.: Reductive materials for remediation of hexavalent chromium contaminated soil – A review, Sci. Total Environ., 773, 145654, https://doi.org/10.1016/J.SCITOTENV.2021.145654, 2021.
Zhang, X., Gai, X., Zhong, Z., Bian, F., Yang, C., Li, Y., and Wen, X.: Understanding variations in soil properties and microbial communities in bamboo plantation soils along a chromium pollution gradient, Ecotoxicol. Environ. Saf., 222, 112507, https://doi.org/10.1016/J.ECOENV.2021.112507, 2021.
Zhang, X., Zhang, X., Li, L., Fu, G., Liu, X., Xing, S., Feng, H., and Chen, B.: The toxicity of hexavalent chromium to soil microbial processes concerning soil properties and aging time, Environ. Res., 204, 111941, https://doi.org/10.1016/J.ENVRES.2021.111941, 2022.
Short summary
Cr pollution is a global concern. The use of methodologies specifically related to Cr toxicity is appropriate, such as the pollution-induced community tolerance (PICT) methodology. The development of PICT was determined in 10 soils after Cr addition in the laboratory. The Cr-soluble fraction and dissolved organic carbon were the main variables determining the development of PICT (R2 = 95.6 %).
Cr pollution is a global concern. The use of methodologies specifically related to Cr toxicity...