Abstract
Polyhalogenated carbazoles (PHCZs) are a kind of emerging contaminants with doxin-like toxicity, potential bioaccumulation capability, and persistence. Data about the risks of PHCZs on soil ecosystem are scarce to date, although PHCZs have been detected with high concentrations in the soil. The present study performed a preliminary investigation of 3,6-dibromocarbazole (36-DBCZ, a PHCZ with a high detection rate, and concentration in the environment) at concentrations of 0.1, 1.0, 10, and 100 mg/kg on the soil health, based on soil enzyme test and Biolog-ECO assay. Results showed that 36-DBCZ could inhibit the activity and diversity of soil microbes, even at the environment-relevant concentration (0.1 mg/kg). But, the inhibition lasted only about 10 days. As time passed, slight increases in microbe activity and diversity were found in 36-DBCZ-treated groups. We hypothesized that the degradation products of 36-DBCZ provided extra nutrients to the soil microbes, which required further verification. Activities of urease, β-glucosidase, and acid phosphatase were increasingly increased, in contrast to the microbial activity. The present study provides valuable data on the effects of PHCZs on the soil ecosystem, and we suggest that the degradation of PHCZs, as well as their influences on the structure and functions of the soil microbial community, should be investigated in future studies.
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The data that support the findings of this study are not openly available and are available from the corresponding author upon reasonable request.
References
Adetunji, A. T., Lewu, F. B., Mulidzi, R., & Ncube, B. (2017). The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: A review. Journal of Soil Science and Plant Nutrition, 17(3), 794–807. https://doi.org/10.4067/S0718-95162017000300018
Busse, M. D., Ratcliff, A. W., Shestak, C. J., & Powers, R. F. (2001). Glyphosate toxicity and the effects of long-term vegetation control on soil microbial communities. Soil Biology & Biochemistry, 33(12–13), 1777–1789. https://doi.org/10.1016/S0038-0717(01)00103-1
Chen, Y. Q., Lin, K. D., Chen, D., Wang, K., Zhou, W. X., Wu, Y., & Huang, X. W. (2018). Formation of environmentally relevant polyhalogenated carbazoles from chloroperoxidase-catalyzed halogenation of carbazole. Environmental Pollution, 232, 264–273. https://doi.org/10.1016/j.envpol.2017.09.045
Cheng, C., Ma, J. C., Wang, J. H., Du, Z. K., Li, B., Wang, J., Gao, C., & Zhu, L. S. (2019). Toxicity comparison of three imidazolium bromide ionic liquids to soil microorganisms. Environmental Pollution, 255, 113321. https://doi.org/10.1016/j.envpol.2019.113321
Eivazi, F., & Tabatabai, M. A. (1988). Glucosidases and galactosidases in soils. Soil Biology & Biochemistry, 20(5), 601–606. https://doi.org/10.1016/0038-0717(88)90141-1
Feigl, V., Eva, U., Emese, V., & Monika, 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
Garland, J. L. (1996). Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biology & Biochemistry, 28(2), 213–221. https://doi.org/10.1016/0038-0717(95)00112-3
Gieg, L. M., Otter, A., & Phillip, M. (1996). Degradation by Pseudomonas sp. LD2: metabolic characteristics and the identification of some metabolites. Environmental Science & Technology, 30(2), 575–585. https://doi.org/10.1021/es950345v
Grigoriadou, A., & Schwarzbauer, J. (2011). Non-target screening of organic contaminants in sediments from the industrial coastal area of Kavala City (NE Greece). Water Air & Soil Pollution, 214(1–4), 623–643. https://doi.org/10.1007/s11270-010-0451-8
Guo, J. H., Chen, D., Potter, D., Rockne, K. J., Sturchio, N. C., Giesy, J. P., & Li, A. (2014). Polyhalogenated carbazoles in sediments of Lake Michigan: A new discovery. Environmental Science & Technology, 48(21), 12807–12815. https://doi.org/10.1021/es503936u
Guo, P. P., Zhu, L. S., Wang, J. H., Wang, J., & Liu, T. (2015). Effects of alkyl-imidazolium ionic liquid [Omim]Cl on the functional diversity of soil microbial communities. Environmental Science and Pollution Research International, 22(12), 9059–9066. https://doi.org/10.1007/s11356-014-4052-8
Ji, C. Y., Shen, C., Zhou, Y. X., Zhu, K. Y., Sun, Z., Zuo, Z. H., & Zhao, M. R. (2019). AhR Agonist Activity Confirmation of Polyhalogenated Carbazoles (PHCZs) Using an Integration of in vitro, in vivo, and in silico models. Environmental Science & Technology, 53(24), 14716–14723. https://doi.org/10.1021/acs.est.9b05388
Kaczynski, P., Lozowicka, B., Hrynko, I., & Wolejko, E. (2016). Behaviour of mesotrione in maize and soil system and its influence on soil dehydrogenase activity. The Science of the Total Environment, 571, 1079–1088. https://doi.org/10.1016/j.scitotenv.2016.07.100
Kandeler, E. (2015). Physiological and biochemical methods for studying soil biota and their functions. In A. Paul (Ed.), Soil microbiology, ecology and biochemistry (4th ed., pp. 187–222). ScienceDirect.
Liu, M. K., Jia, Y. X., Cui, Z. L., Lu, Z. C., Zhang, W. K., Liu, K. Z., Li, S., Shi, L., Ke, R. H., & Lou, Y. H. (2021). Occurrence and potential sources of polyhalogenated carbazoles in farmland soils from the Three Northeast Provinces, China. The Science of the Total Environment, 799, 149459. https://doi.org/10.1016/j.scitotenv.2021.149459
Ma, D., Xie, H. Q., Zhang, W. L., Xue, Q., Liu, X. C., Xu, L., Ma, Y. C., Bonefeld-Jørgensen, E. C., Long, M. H., Zhang, A. Q., & Zhao, B. (2019). Aryl hydrocarbon receptor activity of polyhalogenated carbazoles and the molecular mechanism. The Science of the Total Environment, 687, 516–526. https://doi.org/10.1016/j.scitotenv.2019.05.406
Mumbo, J., Henkelmann, B., Abdelaziz, A., Pfister, G., Nguyen, N., Schroll, R., Munch, J. C., & Schramm, K. W. (2015). Persistence and dioxin-like toxicity of carbazole and chlorocarbazoles in soil. Environmental Science and Pollution Research International, 22(2), 1344–1356. https://doi.org/10.1007/s11356-014-3386-6
Mumbo, J., Pandelova, M., Mertes, F., Henkelmann, B., Bussian, B. M., & Schramm, K. W. (2016). The fingerprints of dioxin-like bromocarbazoles and chlorocarbazoles in selected forest soils in Germany. Chemosphere, 162, 64–72. https://doi.org/10.1016/j.chemosphere.2016.07.056
Parelho, C., Rodrigues, A. S., Barreto, M. C., Ferreira, N. G. C., & Garcia, P. (2016). Assessing microbial activities in metal contaminated agricultural volcanic soils - An integrative approach. Ecotoxicology and Environmental Safety, 129, 242–249. https://doi.org/10.1016/j.ecoenv.2016.03.019.
Parette, R., McCrindle, R., McMahon, K. S., Pena-Abaurrea, M., Reiner, E., Chittim, B., Riddell, N., Voss, G., Dorman, F. L., & Pearson, W. N. (2015). Halogenated indigo dyes: A likely source of 1,3,6,8-tetrabromocarbazole and some other halogenated carbazoles in the environment. Chemosphere, 127, 18–26. https://doi.org/10.1016/j.chemosphere.2015.01.001
Preston-Mafham, J., Boddy, L., & Randerson, P. F. (2006). Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles - A critique. FEMS Microbiology Ecology, 42(1), 1–14. https://doi.org/10.1111/j.1574-6941.2002.tb00990.x
Qiu, Y., Liu, K. Y., Zhou, S. S., Chen, D., Qu, H., Wang, X. D., Hu, Y. X., & Wang, Y. (2019). Polyhalogenated carbazoles in surface sediment from Sanmen Bay, East China Sea: Spatial distribution and congener profile. Bulletin of Environmental Contamination and Toxicology, 103(1), 41–47. https://doi.org/10.1007/s00128-019-02637-7
Schutter, M., & Dick, R. (2001). Shifts in substrate utilization potential and structure of soil microbial communities in response to carbon substrates. Soil Biology & Biochemistry, 33, 1481–1491.
Sun, X., Zhu, L. S., Wang, J. H., Wang, J., Su, B. Y., Liu, T., Zhang, C., Gao, C., & Shao, Y. T. (2017). Toxic effects of ionic liquid 1-octyl-3-methylimidazolium tetrafluoroborate on soil enzyme activity and soil microbial community diversity. Ecotoxicology and Environmental Safety, 135, 201–208. https://doi.org/10.1016/j.ecoenv.2016.09.026
Wang, G. W., Yang, J. K., Gao, S. X., Hou, H. J., Xiao, K. K., Hu, J. P., Liang, S., & Liu, B. C. (2019). New insight into the formation of polyhalogenated carbazoles: Aqueous chlorination of residual carbazole under bromide condition in drinking water. Water Research, 159, 252–261. https://doi.org/10.1016/j.watres.2019.05.015
Wang, G. W., Jiang, T. M., Li, S., Hou, H. J., Xiao, K. K., Hu, J. P., Liang, S., Liu, B. C., & Yang, J. K. (2021). Occurrence and exposure risk evaluation of polyhalogenated carbazoles (PHCZs) in drinking water. Science of the Total Environment, 750, 141615. https://doi.org/10.1016/j.scitotenv.2020.141615
Wu, Y., Qiu, Y. L., Tan, H. L., & Chen, D. (2017). Polyhalogenated carbazoles in sediments from Lake Tai (China): Distribution, congener composition, and toxic equivalent evaluation. Environmental Pollution, 220(Pt A), 142–149. https://doi.org/10.1016/j.envpol.2016.09.032
Xia, X. Y., Zhang, P. P., He, L. L., Gao, X. X., Li, W. J., Zhou, Y. Y., Li, Z. X., Li, H., & Yang, L. (2019). Effects of tillage managements and maize straw returning on soil microbiome using 16S rDNA sequencing. Journal of Integrative Plant Biology, 61(6), 765–777. https://doi.org/10.1111/jipb.12802
Zhang, L., Song, L., Shao, H., Shao, C., Li, M., Liu, M., Brestic, M., & Xu, G. (2014a). Spatio-temporal variation of rhizosphere soil microbial abundance and enzyme activities under different vegetation types in the coastal zone, Shandong, China. Plant Biosystems, 148(3), 403–409. https://doi.org/10.1080/11263504.2013.770804
Zhang, Q. M., Zhu, L. S., Wang, J. H., Xie, H., Wang, J., Wang, F. H., & Sun, F. X. (2014b). Effects of fomesafen on soil enzyme activity, microbial population, and bacterial community composition. Environmental Monitoring and Assessment, 186(5), 2801–2812. https://doi.org/10.1007/s10661-013-3581-9
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This work was supported by the National Natural Science Foundation of China (grant number 41701279) and the China Postdoctoral Science Foundation (grant number 2017M612308).
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Du, Z., Zhang, J., Cheng, C. et al. Effects of 3,6-Dibromocarbazole on Soil Health—Based on Soil Enzymes and the Biolog-ECO Test. Water Air Soil Pollut 233, 256 (2022). https://doi.org/10.1007/s11270-022-05736-0
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DOI: https://doi.org/10.1007/s11270-022-05736-0