Abstract
Arsenic (As) is a soil contaminant with important interactions with the soil microbial community. Upon contamination, soil microbes can display metabolic changes, which can be measured through the profiling of their potential for the oxidation of organic substrates. The present study aimed to evaluate the microbial metabolic profile in soil samples containing different forms of inorganic As (AsIII and AsV) in a 360-day experiment. Soil samples were contaminated with AsIII or AsV (15 mg/kg soil) and the microbial metabolic profile was evaluated after 3, 30, 180, and 360 days of experiment. After these periods, the assay was performed using Biolog Ecoplate™ microplates followed by incubation with readings every 24 h for 5 days. The main parameters evaluated were metabolic activity (AWCD), diversity (Shannon index), and use of substrates containing N or P (NUSE and PUSE). It was observed that the microbial community reacted differently according to the exposure time and for the two contaminants. While metabolic activity decreased in the AsV group (p = 0.03) in 30 days when compared to the control group, the use of sources containing nitrogen decreased in the AsIII group (p = 0.01) only after 360 days when compared to the control group. These findings indicate that the soil microbial community suffers a decrease in metabolic activity when exposed to arsenate in short exposures, whereas, in soil with long-term exposure to arsenite, the microbial community suffers a decrease in the consumption of nitrogen-rich substrates.
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The datasets used and/or analyzed during the current discussion are available and from the corresponding author upon reasonable request.
References
Bakhat, H. F., Zia, Z., Fahad, S., et al. (2017). Arsenic uptake, accumulation and toxicity in rice plants: Possible remedies for its detoxification: A review. Environmental Science and Pollution Research, 24, 9142–9158. https://doi.org/10.1007/S11356-017-8462-2
Blunt, S. M., Sackett, J. D., Rosen, M. R., et al. (2018). Association between degradation of pharmaceuticals and endocrine-disrupting compounds and microbial communities along a treated wastewater effluent gradient in Lake Mead. Science of the Total Environment, 622–623, 1640–1648. https://doi.org/10.1016/J.SCITOTENV.2017.10.052
Boadella, J., Butturini, A., Compte, J., et al. (2021). Different microbial functioning in natural versus man-made Mediterranean coastal lagoons in relation to season. Estuarine, Coastal and Shelf Science, 259, 107434. https://doi.org/10.1016/J.ECSS.2021.107434
Boshoff, M., De Jonge, M., Dardenne, F., et al. (2014). The impact of metal pollution on soil faunal and microbial activity in two grassland ecosystems. Environmental Research, 134, 169–180. https://doi.org/10.1016/J.ENVRES.2014.06.024
Burguera, M., Burguera, J. L., Brunetto, M. R., et al. (1992). Flow-injection atomic spectrometric determination of inorganic arsenic(III) and arsenic(V) species by use of an aluminium-column arsine generator and cold-trapping arsine collection. Analytica Chimica Acta, 261, 105–113. https://doi.org/10.1016/0003-2670(92)80181-6
Candan, E. D., İdil, N., Candan, O. (2021). The microbial community in a green turtle nesting beach in the Mediterranean: Application of the Biolog EcoPlate approach for beach pollution. Environmental Science and Pollution Research 28, 49685–49696. https://doi.org/10.1007/S11356-021-14196-8
Chen, X., Zeng, X. C., Kawa, Y. K., et al. (2020). Microbial reactions and environmental factors affecting the dissolution and release of arsenic in the severely contaminated soils under anaerobic or aerobic conditions. Ecotoxicology and Environmental Safety, 189, 109946. https://doi.org/10.1016/J.ECOENV.2019.109946
CONAMA (2009) Conselho Nacional do Meio Ambiente Resolução no420, de 28 de dezembro de 2009. Dispõe sobre critérios e valores orientadores de qualidade do solo quanto à presença de substâncias químicas e estabelece diretrizes para o gerenciamento ambiental de áreas contaminadas por essas substâncias em decorrência de atividades antrópicas. Diário Oficial da República Federativa do Brasil, Poder Executivo, Brasília, DF, 30 dez. 2009. Seção 1, 20p. https://www.ibama.gov.br/component/legislacao/?view=legislacao&force=1&legislacao=115509
da Silva, E. B., Gao, P., Xu, M., et al. (2020). Background concentrations of trace metals As, Ba, Cd Co, Cu, Ni, Pb, Se, and Zn in 214 Florida urban soils: Different cities and land uses. Environmental Pollution, 264, 114737. https://doi.org/10.1016/J.ENVPOL.2020.114737
Da Silva Júnior, F. M. R., Rocha, J. A. V., & Vargas, V. M. F. (2009). Extraction parameters in the mutagenicity assay of soil samples. Science of The Total Environment, 407(23), 6017-6023. https://doi.org/10.1016/j.scitotenv.2009.08.021
Da Silva Júnior, F. M. R., Volcão, L. M., Hoscha, L. C., & Pereira, S. V. (2018). Growth of the fungus Chaetomium aureum in the presence of lead: Implications in bioremediation. Environmental Earth Sciences, 77(7), 275. https://doi.org/10.1007/s12665-018-7447-x
Dincă, L. C., Grenni, P., Onet, C., & Onet, A. (2022). Fertilization and soil microbial community: A review. Applied Sciences, 12, 1198. https://doi.org/10.3390/APP12031198
Domeignoz-Horta, L. A., Pold, G., Liu, X. J. A., et al. (2020). Microbial diversity drives carbon use efficiency in a model soil. Nature Communications, 11, 1–10. https://doi.org/10.1038/s41467-020-17502-z
Dunivin, T. K., Yeh, S. Y., & Shade, A. (2019). A global survey of arsenic-related genes in soil microbiomes. BMC Biology, 17, 1–17. https://doi.org/10.1186/S12915-019-0661-5/FIGURES/8
Feigl, V., Ujaczki, É., Vaszita, E., & Molnár, M. (2017). Influence of red mud on soil microbial communities: Application and comprehensive evaluation of the Biolog EcoPlate approach as a tool in soil microbiological studies. Science of the Total Environment, 595, 903–911. https://doi.org/10.1016/J.SCITOTENV.2017.03.266
Floch, C., Chevremont, A.-C., Joanico, K., et al. (2011). Indicators of pesticide contamination: Soil enzyme compared to functional diversity of bacterial communities via Biolog® Ecoplates. European Journal of Soil Biology, 47, 256–263. https://doi.org/10.1016/j.ejsobi.2011.05.007
Furtak K, Gawryjołek K, Gajda A, Gałązka A (2017). Effects of maize and winter wheat grown under different cultivation techniques on biological activity of soil. Plant, Soil and Environment 63:449–454. https://doi.org/10.17221/486/2017-PSE
Gałązka, A., & Grządziel, J. (2018). Fungal genetics and functional diversity of microbial communities in the soil under long-term monoculture of maize using different cultivation techniques. Frontiers in Microbiology, 9, 76. https://doi.org/10.3389/FMICB.2018.00076
Garland, J. L., & Mills, A. L. (1991). Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Applied and Environmental Microbiology, 57(8), 2351–2359. https://doi.org/10.1128/aem.57.8.2351-2359.1991
Gryta, A., Frąc, M., & Oszust, K. (2014). The application of the Biolog EcoPlate approach in ecotoxicological evaluation of dairy sewage sludge. Applied Biochemistry and Biotechnology, 174, 1434–1443. https://doi.org/10.1007/S12010-014-1131-8
Hanaka, A., Ozimek, E., Majewska, M., et al. (2019). Physiological diversity of Spitsbergen soil microbial communities suggests their potential as plant growth-promoting bacteria. International Journal of Molecular Sciences, 20, 1207. https://doi.org/10.3390/IJMS20051207
Honscha, L. C., Campos, A. S., Tavella, R. A., et al. (2021). Bioassays for the evaluation of reclaimed opencast coal mining areas. Environmental Science and Pollution Research, 28, 26664–26676. https://doi.org/10.1007/S11356-021-12424-9
Huang, J.-H. (2014). Impact of microorganisms on arsenic biogeochemistry: A review. Water, Air, and Soil Pollution, 225, 1–25. https://doi.org/10.1007/S11270-013-1848-Y
Islam, M. R., Chauhan, P. S., Kim, Y., et al. (2010). Community level functional diversity and enzyme activities in paddy soils under different long-term fertilizer management practices. Biology and Fertility of Soils, 47, 599–604. https://doi.org/10.1007/S00374-010-0524-2
Koner, S., Chen, J. S., Hsu, B. M., et al. (2022). Depth-resolved microbial diversity and functional profiles of trichloroethylene-contaminated soils for Biolog EcoPlate-based biostimulation strategy. Journal of Hazardous Materials, 424, 127266. https://doi.org/10.1016/J.JHAZMAT.2021.127266
Kuivenhoven, M., Mason, K. (2021). Arsenic Toxicity. In: StatPearls. StatPearls Publishing, Treasure Island (FL).
Lee L-H, Letchumanan V, Mutalib N-SA, Cheah YK (2017). Microbial community diversity in the soil of Barrientos Island estimated by RAPD and Biolog Ecoplate methods. Progress in Microbes and Molecular Biology 3(1):10 https://doi.org/10.36877/PMMB.A0000046
Liu, B., Li, Y., Zhang, X., et al. (2015). Effects of chlortetracycline on soil microbial communities: Comparisons of enzyme activities to the functional diversity via Biolog EcoPlatesTM. European Journal of Soil Biology, 68, 69–76. https://doi.org/10.1016/J.EJSOBI.2015.01.002
Liu, C., Lin, H., Dong, Y., et al. (2018). Investigation on microbial community in remediation of lead-contaminated soil by Trifolium repensL. Ecotoxicology and Environmental Safety, 165, 52–60. https://doi.org/10.1016/J.ECOENV.2018.08.054
Lv, T., Carvalho, P. N., Zhang, L., et al. (2017). Functionality of microbial communities in constructed wetlands used for pesticide remediation: Influence of system design and sampling strategy. Water Research, 110, 241–251. https://doi.org/10.1016/J.WATRES.2016.12.021
Mandal, B. K., & Suzuki, K. T. (2002). Arsenic round the world: A review. Talanta, 58, 201–235. https://doi.org/10.1016/S0039-9140(02)00268-0
Matta, G., & Gjyli, L. (2016). Mercury, lead and arsenic: Impact on environment and human health. Journal of Chemical and Pharmaceutical Sciences, 9, 718–725.
Muszyńska, E., & Labudda, M. (2019). Dual role of metallic trace elements in stress biology—From negative to beneficial impact on plants. International Journal of Molecular Sciences, 20, 3117. https://doi.org/10.3390/IJMS20133117
Németh, I., Molnár, S., Vaszita, E., & Molnár, M. (2021). The Biolog EcoPlateTM technique for assessing the effect of metal oxide nanoparticles on freshwater microbial communities. Nanomaterials, 11, 1777. https://doi.org/10.3390/NANO11071777
Pass, D. A., Morgan, A. J., Read, D. S., et al. (2015). The effect of anthropogenic arsenic contamination on the earthworm microbiome. Environmental Microbiology, 17, 1884–1896. https://doi.org/10.1111/1462-2920.12712
Pitombo, L. M., Ramos, J. C., Quevedo, H. D., et al. (2018). Methodology for soil respirometric assays: Step by step and guidelines to measure fluxes of trace gases using microcosms. MethodsX, 5, 656–668. https://doi.org/10.1016/J.MEX.2018.06.008
Rahman, Z., & Singh, V. P. (2019). The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: An overview. Environmental Monitoring and Assessment, 191, 1–21. https://doi.org/10.1007/S10661-019-7528-7/TABLES/3
Ramires, P. F., Tavella, R. A., Escarrone, A. L., et al. (2021). Ecotoxicity of triclosan in soil: An approach using different species. Environmental Science and Pollution Research, 28, 41233–41241. https://doi.org/10.1007/s11356-021-13633-y
Sala, M. M., Pinhassi, J., & Gasol, J. M. (2006). Estimation of bacterial use of dissolved organic nitrogen compounds in aquatic ecosystems using Biolog plates. Aquatic Microbial Ecology, 42, 1–5. https://doi.org/10.3354/AME042001
Schloter, M., Nannipieri, P., Sørensen, S. J., & van Elsas, J. D. (2018). Microbial indicators for soil quality. Biology and Fertility of Soils, 54, 1–10. https://doi.org/10.1007/S00374-017-1248-3/FIGURES/1
Sethi, S., & Gupta, P. (2020). Soil contamination: A menace to life. Soil Contam - Threat Sustain Solut. https://doi.org/10.5772/INTECHOPEN.94280
Silva, M. G., Volcão, L. M., Seus, E. R., Machado, M. I., Mirlean, N., Baisch, P. R. M., & da Silva Júnior, F. M. R. (2022). Comparative evaluation of different bioremediation techniques for crude oil-contaminated soil. International Journal of Environmental Science and Technology, 19(4), 2823–2834. https://doi.org/10.1007/s13762-021-03325-y
Sisinno CLS, Oliveira-Filho EC (2013). Princípios de toxicologia ambiental. Ed Interciência 198
Tchounwou, P. B., Yedjou, C. G., Udensi, U. K., et al. (2019). State of the science review of the health effects of inorganic arsenic: Perspectives for future research. Environmental Toxicology, 34, 188–202. https://doi.org/10.1002/TOX.22673
Volcão, L. M., Fraga, L. S., de Lima, B. R., et al. (2020). Toxicity of biocide formulations in the soil to the gut community in Balloniscus selowii Brandt, 1983 (Crustacea: Isopoda: Oniscidea). Water, Air, and Soil Pollution, 231, 1–8. https://doi.org/10.1007/s11270-020-04689-6
Wei, D., Yang, Q., Zhang, J. Z., et al. (2008). Bacterial community structure and diversity in a black soil as affected by long-term fertilization. Pedosphere, 18, 582–592. https://doi.org/10.1016/S1002-0160(08)60052-1
Xu, W., Ge, Z., & Poudel, D. R. (2015). Application and optimization of Biolog EcoPlates in functional diversity studies of soil microbial communities. MATEC Web Conf, 22, 04015. https://doi.org/10.1051/MATECCONF/20152204015
Yu, Z., Liu, X., Zeng, X., et al. (2020). Effect of arsenic pollution extent on microbial community in Shimen long-term arsenic-contaminated soil. Water, Air, and Soil Pollution, 231, 1–11. https://doi.org/10.1007/S11270-020-04716-6
Zhang, S., Liu, X., Jiang, Q., et al. (2017). Legacy effects of continuous chloropicrin-fumigation for 3-years on soil microbial community composition and metabolic activity. AMB Express, 7, 1–11. https://doi.org/10.1186/S13568-017-0475-1
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and Conselho Nacional de Desenvolvimento Científico e Tecnológico – Grant 310856/2020–5 and Grant 408303/2018–2.
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Rodrigo Brum: conceptualization, data curation, formal analysis, investigation, methodology, roles/writing—original draft, writing—review and editing; Lisiane Volcão: conceptualization, formal analysis, methodology, writing—review and editing; Livia Freitas: writing—review and editing; Jessica Santos: writing—review and editing; Mariana Coronas: conceptualization, writing—review and editing; Juliane Ventura-Lima: conceptualization, writing—review and editing; Daiane Dias: conceptualization, writing—review and editing; Bruno Soares: conceptualization, writing—review and editing; Erico Corrêa: conceptualization, writing—review and editing; Ng Haig They: conceptualization, writing—review and editing; Daniela Ramos: conceptualization,m writing—review and editing; Flavio da Silva Júnior: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, supervision, visualization, writing—review and editing.
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de Lima Brum, R., Volcão, L.M., da Silva Freitas, L. et al. Metabolic Profile of the Soil Microbial Community Exposed to Arsenite and Arsenate: a 1-Year Experiment. Water Air Soil Pollut 233, 317 (2022). https://doi.org/10.1007/s11270-022-05825-0
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DOI: https://doi.org/10.1007/s11270-022-05825-0