Abstract
The production of toxic sulfides is a common environmental problem in mariculture. Therefore, the effective inhibition of sulfidogens is the key to prevent sulfides production. In this study, the possibility and mechanism of nitrate (NO3−) inhibiting the activity of the sulfate-reducing microbiota (SRM) from mariculture sediments was investigated. The results showed that 1, 3, and 5 mmol L−1 NO3− continuously inhibited sulfide production for 1–3 d. As NO3− dosage increased to 7 mmol L−1, the duration of inhibition increased to 6 days. Denitrifying product NO2− heavily inhibited the activity of dissimilar sulfate reductase gene (dsrB) by 3 orders, which was the main reason that the sulfate-reducing activity was inhibited. The SRM structure changed significantly with the dosage of NO3−, while the abundance of sulfidogens Desulfovibrio species increased due to their capability of detoxifying nitrite through nitrite reductase. Hence, sulfidogens Desulfovibrio species are more adaptable to a high nitrate/nitrite environment, and the traditional control strategies by dosing nitrate/nitrite should be paid more attention to. The findings will serve as helpful guidelines for sulfate-reducing microbiota in the habitat of mariculture to reduce their generation of poisonous sulfide.
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References
Boetius, A., Ravenschlag, K., Schubert, C. J., Rickert, D., Widdel, F., Gieseke, A., et al., 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407: 623–626.
Chen, Y., Wang, J., Zhao, Y. G., Maqbool, F., Gao, M., Guo, L., et al., 2022. Sulfamethoxazole removal from mariculture wastewater in moving bed biofilm reactor and insight into the changes of antibiotic and resistance genes. Chemosphere, 298: 134327.
Darwin, A., Hussain, H., Griffiths, L., Grove, J., Sambongi, Y., Busby, S., et al., 1993. Regulation and sequence of the structural gene for cytochrome C552 from Escherichia coli: Not a hexahaem but a 50 kDa tetrahaem nitrite reductase. Molecular Microbiology, 9: 1255–1265.
de Andrade, J. S., Vieira, M. R. S., Oliveira, S. H., de Melo Santos, S. K., and Urtiga Filho, S. L., 2020. Study of microbiologically induced corrosion of 5052 aluminum alloy by sulfate-reducing bacteria in seawater. Materials Chemistry and Physics, 241: 122296.
Eckford, R. E., and Fedorak, P. M., 2002. Planktonic nitrate-reducing bacteria and sulfate-reducing bacteria in some western Canadian oil field waters. Journal of Industrial Microbiology and Biotechnology, 29: 83–92.
Fan, F., Zhang, B., Liu, J., Cai, Q., Lin, W., and Chen, B., 2020. Towards sulfide removal and sulfate reducing bacteria inhibition: Function of biosurfactants produced by indigenous isolated nitrate reducing bacteria. Chemosphere, 238: 124655.
Gao, C., Wang, A., Wu, W. M., Yin, Y., and Zhao, Y. G., 2014. Enrichment of anodic biofilm inoculated with anaerobic or aerobic sludge in single chambered air-cathode microbial fuel cells. Bioresource Technology, 167: 124–132.
Haveman, S. A., Greene, E. A., and Voordouw, G., 2005. Gene expression analysis of the mechanism of inhibition of Desulfovibrio vulgaris Hildenborough by nitrate-reducing, sulfide-oxidizing bacteria. Environmental Microbiology, 7: 1461–1465.
Hu, X., Liu, J., Liu, H., Zhuang, G., and Xun, L., 2018. Sulfur metabolism by marine heterotrophic bacteria involved in sulfur cycling in the ocean. Science China Earth Sciences, 61: 1369–1378.
Jørgensen, B. B., 1977. The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnology and Oceanography, 22: 814–832.
Jørgensen, B. B., 1982. Mineralization of organic matter in the sea bed–The role of sulphate reduction. Nature, 296: 643–645.
Kang, P., and Xu, S., 2016. The impact of mariculture on nutrient dynamics and identification of the nitrate sources in coastal waters. Environmental Science and Pollution Research, 23: 1300–1311.
Korte, H. L., Fels, S. R., Christensen, G. A., Price, M. N., Kuehl, J. V., Zane, G. M., et al., 2014. Genetic basis for nitrate resistance in Desulfovibrio strains. Frontiers in Microbiology, 5: 153.
Korte, H. L., Saini, A., Trotter, V. V., Butland, G. P., Arkin, A. P., and Wall, J. D., 2015. Independence of nitrate and nitrite inhibition of Desulfovibrio vulgaris hildenborough and use of nitrite as a substrate for growth. Environmental Science and Technology, 49: 924–931.
Kumar, S. S., Malyan, S. K., Basu, S., and Bishnoi, N. R., 2017. Syntrophic association and performance of Clostridium, De-Sulfovibrio, Aeromonas and Tetrathiobacter as anodic biocatalysts for bioelectricity generation in dual chamber microbial fuel cell. Environmental Science and Pollution Research, 24: 16019–16030.
Lai, R., Li, Q., Cheng, C., Shen, H., Liu, S., Luo, Y., et al., 2020. Bio-competitive exclusion of sulfate-reducing bacteria and its anticorrosion property. Journal of Petroleum Science and Engineering, 194: 107480.
Liu, H., Tan, S., Yu, T., and Liu, Y., 2016. Sulfate reducing bacterial community and in situ activity in mature fine tailings analyzed by real time qPCR and microsensor. Journal of Environmental Sciences, 44: 141–147.
Meng, T., Zhu, M. X., Ma, W. W., and Gan, Z. X., 2019. Sulfur, iron, and phosphorus geochemistry in an intertidal mudflat impacted by shellfish aquaculture. Environmental Science and Pollution Research, 26: 6460–6471.
Meyer, B., Kuehl, J. V., Deutschbauer, A. M., Arkin, A. P., and Stahl, D. A., 2013. Flexibility of syntrophic enzyme systems in Desulfovibrio species ensures their adaptation capability to environmental changes. Journal of Bacteriology, 195: 4900–4914.
Myhr, S., Lillebø, B. L., Sunde, E., Beeder, J., and Torsvik, T., 2002. Inhibition of microbial H2S production in an oil reservoir model column by nitrate injection. Applied Journal of Microbiology and Biotechnology, 58: 400–408.
Okabe, S., Ito, T., Satoh, H., and Watanabe, Y., 2003. Effect of nitrite and nitrate on biogenic sulfide production in sewer biofilms determined by the use of microelectrodes. Water Science and Technology, 47: 281–288.
Pandey, C. B., Kumar, U., Kaviraj, M., Minick, K. J., Mishra, A. K., and Singh, J. S., 2020. DNRA: A short-circuit in biological N-cycling to conserve nitrogen in terrestrial ecosystems. Science of the Total Environment, 738: 139710.
Pillay, C., and Lin, J., 2013. Metal corrosion by aerobic bacteria isolated from stimulated corrosion systems: Effects of additional nitrate sources. International Biodeterioration and Biodegradation, 83: 158–165.
Pozsgai, G., Bátai, I. Z., and Pintér, E., 2019. Effects of sulfide and polysulfides transmitted by direct or signal transduction-mediated activation of TRPA1 channels. British Journal of Pharmacology, 176: 628–645.
Price, M. N., Deutschbauer, A. M., Kuehl, J. V., Liu, H., Witkowska, H. E., and Arkin, A. P., 2011. Evidence-based annotation of transcripts and proteins in the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Journal of Bacteriology, 193: 5716–5727.
Qi, P., Sun, D., Zhang, G., Li, D., Wu, T., and Li, Y., 2022. Bio-augmentation with dissimilatory nitrate reduction to ammonium (DNRA) driven sulfide-oxidizing bacteria enhances the durability of nitrate-mediated souring control. Water Reseach, 219: 118556.
San Diego-McGlone, M. L., Azanza, R. V., Villanoy, C. L., and Jacinto, G. S., 2008. Eutrophic waters, algal bloom and fish kill in fish farming areas in Bolinao, Pangasinan, Philippines. Marine Pollution Bulletin, 57: 295–301.
Schink, B., and Pfennig, N., 1982. Propionigenium modestum gen. nov. sp. nov. a new strictly anaerobic, nonsporing bacterium growing on succinate. Archives of Microbiology, 133: 209–216.
Shivani, Y., Subhash, Y., Sasikala, C., and Ramana, C. V., 2017. Halodesulfovibrio spirochaetisodalis gen. nov. sp. nov. and reclassification of four Desulfovibrio spp. International Journal of Systematic and Evolutionary Microbiology, 67: 87–93.
Steenkamp, D. J., and Peck, H. D., 1981. Proton translocation associated with nitrite respiration in Desulfovibrio desulfuricans. Journal of Biological Chemistry, 256: 5450–5458.
Thomas, Y., Courties, C., El Helwe, Y., Herbland, A., and Lemonnier, H., 2010. Spatial and temporal extension of eutrophication associated with shrimp farm wastewater discharges in the New Caledonia lagoon. Marine Pollution Bulletin, 61: 387–398.
Wang, X., Wang, J., Zhao, Y. G., Maqbool, F., Guo, L., Gao, M., et al., 2021. Control of toxic sulfide in mariculture environment by iron-coated ceramsite and immobilized sulfur oxidizing bacteria. Science of the Total Environment, 12: 148658.
Wen, J., Zhao, K., Gu, T., and Raad, I. I., 2009. A green biocide enhancer for the treatment of sulfate-reducing bacteria (SRB) biofilms on carbon steel surfaces using glutaraldehyde. International Biodeterioration and Biodegradation, 63: 1102–1106.
Wu, J., Lu, J., Wen, X., Zhang, Z., and Lin, Y., 2019. Severe nitrate pollution and health risks of coastal aquifer simultaneously influenced by saltwater intrusion and intensive anthropogenic activities. Archives of Environmental Contamination and Toxicology, 77: 79–87.
Xin, M., Wang, B., Xie, L., Sun, X., Wei, Q., Liang, S., et al., 2019. Long-term changes in nutrient regimes and their ecological effects in the Bohai Sea, China. Marine Pollution Bulletin, 146: 562–573.
Xu, J., Han, L., and Yin, W., 2022. Research on the ecologicalization efficiency of mariculture industry in China and its influencing factors. Marine Policy, 137: 104935.
Yan, S., Cheng, K. Y., Ginige, M. P., Morris, C., Deng, X., Li, J., et al., 2022. Sequential removal of selenate, nitrate and sulfate and recovery of elemental selenium in a multi-stage bioreactor process with redox potential feedback control. Journal of Hazardous Materials, 424: 127539.
Zhou, C., Vannela, R., Hayes, K. F., and Rittmann, B. E., 2014. Effect of growth conditions on microbial activity and iron-sulfide production by Desulfovibrio vulgaris. Journal of Hazardous Materials, 272: 28–35.
Zhou, J., and Xing, J., 2021. Haloalkaliphilic denitrifiers-dependent sulfate-reducing bacteria thrive in nitrate-enriched environments. Water Reseach, 201: 117354.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (No. 41977315), and the Funda- mental Research Funds for the Central Universities of China (No. 201964004).
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Zhao, X., Zhang, Z., Zhao, Y. et al. Insight into the Inhibition of the Poisonous Sulfide Production from Sulfate-Reducing Microbiota in Mariculture Habitat. J. Ocean Univ. China 23, 447–454 (2024). https://doi.org/10.1007/s11802-024-5539-7
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DOI: https://doi.org/10.1007/s11802-024-5539-7