Biotoxicity of NH4+ on Nostoc Sphaeroides (diazotrophic cyanobacteria) in paddy floodwater

Jihai Shao; Li Fan; Ye Feng

doi:10.26789/AEB.2023.01.005

Biotoxicity of NH4+ on Nostoc Sphaeroides (diazotrophic cyanobacteria) in paddy floodwater

VIEWS - 318 (Abstract) 145 (PDF)

Jihai Shao, Li Fan, Ye Feng

Abstract

In order to elucidate the toxicity of NH₄⁺ on Nostoc Sphaeroides (commonly named GE-XIAN-MI in China, GXM), a diazotrophic cyanobacterium in paddy fields, this study investigated the growth, photosynthesis, N₂-fixation, and oxidative-antioxidative characteristics of GXM under NH₄⁺stress in paddy floodwater. The results showed that the photosynthesis and the N₂-fixing ability of GXM were inhibited by NH₄⁺ at a concentration of 13.46 mg L^-1 in paddy floodwater. The main target of NH₄⁺ on photosystem II (PS II) of GXM was the electron donor side of react center. Oxygen evolution complex (OEC) was the secondary target of toxicity of NH₄⁺ on PS II. The damage of PS II led to accumulation of ROS and resulted in oxidative damage on plasma membrane of GXM. Feedback inhibition and decrease of photosynthetic energy production may be the reasons for the decrease of N₂-fixing ability of GXM under NH₄⁺ stress. The results presented in this study suggest that high level of NH₄⁺ loading may be a reason for the recession of GXM resource in paddy fields.

Keywords

Nostoc Sphaeroides; Ammonium; Paddy floodwater; Photosynthesis; Nitrogenase; Oxidative damage

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References

Abinandan, S., Subashchandrabose, S.R., Venkateswarlu, K., Megharaj M., 2019. Soil microalgae and cyanobacteria: the biotechnological potential in the maintenance of soil fertility and health. Critical reviews in biotechnology, 39 (8): 981-998.

https://doi.org/10.1080/07388551.2019.1654972

Akoijam, C., Langpoklakpam, J.S., Chettri, B., Singh, A.K., 2015. Cyanobacterial diversity in hydrocarbon-polluted sediments and their possible role in bioremediation. International Biodeterioration & Biodegradation, 103: 97-104.

https://doi.org/10.1016/j.ibiod.2015.03.035

Chen, P., Xu, J., Zhang, Z., Nie, T., 2022. 'Preferential' ammonium uptake by rice does not always turn into higher N recovery of fertilizer sources under water-saving irrigation. Agricultural Water Management, 272: 107867.

https://doi.org/10.1016/j.agwat.2022.107867

Christen, D., Schönmann, S., Jermini, M., Strasser, R.J., Défago, G., 2007. Characterization and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. Environmental and Experimental Botany, 60(3): 504-514.

https://doi.org/10.1016/j.envexpbot.2007.02.003

Dagnino-Leone, J., Figueroa, C.P., Castañeda, M.L., Youlton, A.D., Vallejos-Almirall, A., Agurto-Muñoz, A., Pérez, J.P., Agurto-Muñoz, C., 2022. Phycobiliproteins: Structural aspects, functional characteristics, and biotechnological perspectives. Computational and Structural Biotechnology Journal, 20: 1506-1527.

https://doi.org/10.1016/j.csbj.2022.02.016

Dai, G., Deblois, C.P., Liu, S., Juneau, P., Qiu, B., 2008. Differential sensitivity of five cyanobacterial strains to ammonium toxicity and its inhibitory mechanism on the photosynthesis of rice-field cyanobacterium Ge-Xian-Mi (Nostoc). Aquatic Toxicology, 89 (2): 113-121.

https://doi.org/10.1016/j.aquatox.2008.06.007

Dekaezemacker, J. and Bonnet, S., 2011. Sensitivity of N2 fixation to combined nitrogen forms (NO3− and NH4+) in two strains of the marine diazotroph Crocosphaera watsonii (Cyanobacteria). Marine Ecology Progress Series, 438: 33-46.

https://doi.org/10.3354/meps09297

Del Rio, D., Stewart, A.J., Pellegrini, N., 2005. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutrition, metabolism and cardiovascular diseases, 15(4): 316-328.

https://doi.org/10.1016/j.numecd.2005.05.003

Drath, M., Kloft, N., Batschauer, A., Marin, K., Novak, J., Forchhammer, K., 2008. Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant physiology, 147(1): 206–215.

https://doi.org/10.1104/pp.108.117218

Evans, M.C., Ball, R.J., Nugent, J.H., 2005. Ammonia displaces methanol bound to the water oxidizing complex of photosystem II in the S2 state. FEBS letters, 579(14): 3081-3084.

https://doi.org/10.1016/j.febslet.2005.04.066

Feng, Y., 2023. Evaluation of biotoxicity of NH4+ on paddy diazotrophic cyanobacteria GE-XIAN-MI (Nostoc Sphaeroides) based on statistical analyses using SPSS. Model World, 4: 163-165.

Gheda, S.F. and Ahmed, D.A., 2015. Improved soil characteristics and wheat germination as influenced by inoculation of Nostoc kihlmani and Anabaena cylindrica. Rendiconti Lincei, 26: 121-131.

https://doi.org/10.1007/s12210-014-0351-8

Glazer, A.N., 1984. Phycobilisome a macromolecular complex optimized for light energy transfer. Biochimica et Biophysica Acta (BBA)-Reviews on Bioenergetics, 768(1): 29-51.

https://doi.org/10.1016/0304-4173(84)90006-5

Guo, J.H., Liu, X.J., Zhang, Y., Shen, J.L., Han, W.X., Zhang, W.F., Christie, P., Goulding, K.W.T., Vitousek, P.M., Zhang, F.S., 2010. Significant acidification in major Chinese croplands. Science, 327(5968): 1008-1010.

https://doi.org/10.1126/science.1182570

Hong, Y., Hu, H. Y., Li, F.M., 2008. Physiological and biochemical effects of allelochemical ethyl 2-methyl acetoacetate (EMA) on cyanobacterium Microcystis aeruginosa. Ecotoxicology and environmental safety, 71(2): 527-534.

https://doi.org/10.1016/j.ecoenv.2007.10.010

Hu, T., Chen, A., Jiang, Y., Sun, C., Sun, C., Luo, S., Shao, J., 2022. Application of a newly recorded diazotrophic cyanobacterium in acidified and Cd contaminated paddy soil: Promotes rice yield and decreases Cd accumulation. Science of The Total Environment, 814: 152630.

https://doi.org/10.1016/j.scitotenv.2021.152630

Jadhav, S.B., Phugare, S.S., Patil, P.S., Jadhav, J.P., 2011. Biochemical degradation pathway of textile dye remazol red and subsequent toxicological evaluation by cytotoxicity, genotoxicity and oxidative stress studies. International Biodeterioration & Biodegradation, 65(6): 733-743.

https://doi.org/10.1016/j.ibiod.2011.04.003

Jiang, Y., Hu, T., Peng, O., Chen, A., Tie, B., Shao, J., 2022. Impact of heavy metal passivators on the nitrogenase activity and diazotrophic community in a cadmium-contaminated paddy field. International Biodeterioration & Biodegradation, 175: 105506.

https://doi.org/10.1016/j.ibiod.2022.105506

Jiang, Y., Hu, T., Peng, O., Chen, A., Tie, B., Shao, J., 2021. Responses of microbial community and soil enzyme to heavy metal passivators in cadmium contaminated paddy soils: An in situ field experiment. International Biodeterioration & Biodegradation, 164: 105292.

https://doi.org/10.1016/j.ibiod.2021.105292

Källqvist, T. and Svenson, A., 2003. Assessment of ammonia toxicity in tests with the microalga, Nephroselmis pyriformis, Chlorophyta. Water Research, 37: 477-484

Kater, B.J., Dubbeldam, M., Postma, J.F., 2006. Ammonium toxicity at high pH in a marine bioassay using Corophium volutator. Archives of environmental contamination and toxicology, 51(3): 347–351.

https://doi.org/10.1007/s00244-005-0163-z

Khorobrykh, S., Havurinne, V., Mattila, H., Tyystjärvi, E., 2020. Oxygen and ROS in Photosynthesis. Plants (Basel, Switzerland), 9(1): 91.

https://doi.org/10.3390/plants9010091

Lin, Y., Chen, A., He, Y., Qing, C., Peng, L., Luo, S., Shao, J., 2019. Responses of Microcystis aeruginosa (Cyanobacteria) to sanguinarine stress: morphological and physiological characteristics associated with competitive advantage. Phycologia, 58(3): 260-268.

https://doi.org/10.1080/00318884.2018.1561966

Lin, Y., Chen, A., Wu, G., Peng, L., Xu, Z., Shao, J., 2017. Growth, microcystins synthesis, and cell viability of Microcystis aeruginosa FACHB905 to dissolved organic matter originated from cattle manure. International Biodeterioration & Biodegradation, 118: 126-133.

https://doi.org/10.1016/j.ibiod.2017.01.031

Liu, D., Ma, J., Cheng, M., Wu, N., Xue, L., Zhao, C., 2020. Study on the effect of CO2 leakage on the basic water quality index of paddy field water. Acta Scientiae Circumstantiae, 40: 1298-1308.

https://doi.org/10.13671/j.hjkxxb.2019.0484

Lü, Y., Zheng, M., Wu, J., Wu, P., Lao, J., Fu, W., 2022. Effects of different nitrogen reduction fertilizer combined with milk vetch (Astragalus sinicus L.) on the loss of nitrogen and phosphorus in field water and rice growth. Journal of Soil and Water Conservation, 36: 148-155.

https://doi.org/10.13870/j.cnki.stbcxb.2022.06.019

Moisander, P.H., Daley, M.C., Shoemaker, K.M., Kolte, V., Sharma, G., Garlick, K., 2022. Nitrogen fixation influenced by phosphorus and nitrogen availability in the benthic bloom-forming cyanobacterium Hydrocoleum sp. identified in a temperate marine lagoon. Journal of Phycology, 2022, 58(3): 377-391.

https://doi.org/10.1111/jpy.13244

Moustakas, M., 2022. Plant photochemistry, reactive oxygen species, and photoprotection. Photochemistry, 2: 5-8.

https://doi.org/10.3390/photochem2010002

Qin, H., Lu, J., Wang, Z., Li, D., 2013. The influence of soil and water physicochemical properties on the distribution of nostoc sphaeroides (cyanophyceae) in paddy fields and biochemical comparison with indoor cultured biomass. Journal of Applied Phycology, 25: 1737-1745.

https://doi.org/10.1007/s10811-013-0040-5

Qing, C., Zhang, H., Chen, A., Lin, Y., Shao, J., 2020. Effects and possible mechanisms of sanguinarine on the competition between Raphidiopsis raciborskii (Cyanophyta) and Scenedesmus obliquus (Chlorophyta): A comparative toxicological study. Ecotoxicology and Environmental Safety, 206: 111192.

https://doi.org/10.1016/j.ecoenv.2020.111192

Shao, J., Yan, Q., Sun, C., Sun, C., Feng, Y., Miao, K., Wang, S., 2021. Cattle manure DOM on adsorption of copper by the cyanobacterium Aliinostoc species. Applied Environmental Biotechnology, 6(2): 13-18.

https://doi.org/10.26789/AEB.2021.02.002

Sharma, V., Prasanna, R., Hossain, F., Muthusamy, V., Nain, L., Das, S., Shivay, Y.S., Kumar, A., 2020. Priming maize seeds with cyanobacteria enhances seed vigour and plant growth in elite maize inbreds. Biotechnology, 10(4): 154.

https://doi.org/10.1007/s13205-020-2141-6

Shrestha, J., Karki, T.B., Hossain, M.A., 2022. Application of nitrogenous fertilizer in rice production: A review. Journal of Nepal Agricultural Research Council, 8: 16-26.

https://doi.org/10.3126/jnarc.v8i.44815

Sies, H., Belousov, V.V., Chandel, N.S. Davies, M.J., Jones, D.P., Mann, G.E., Murphy, M.P., Yamamoto, M., Winterbourn, C.., 2022. Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nature Reviews Molecular Cell Biology, 23: 499-515.

https://doi.org/10.1038/s41580-022-00456-z

Subramanian, G., Sekar, S., Sampoornam, S., 1994. Biodegradation and utilization of organophosphorus pesticides by cyanobacteria. International biodeterioration & biodegradation, 33(2): 129-143.

https://doi.org/10.1016/0964-8305(94)90032-9

Yan, Q., Xiao, P., Li, J., He, Y., Shao, J., 2022. Physiological responses of a diazotrophic cyanobacterium to acidification of paddy floodwater: N2 fixation, Photosynthesis, and Oxidative–Antioxidative Characteristics. International Journal of Environmental Research and Public Health, 19(22): 15070.

https://doi.org/10.3390/ijerph192215070

Yan, X., Zhao, F., Wang, G., Wang, Z., Zhou, M., Zhang, L., Wang, G., Chen, Y., 2023. Metabolomic analysis of Microcystis aeruginosa after exposure to the algicide L-lysine. Bulletin of Environmental Contamination and Toxicology, 110(1): 1-7.

https://doi.org/10.1007/s00128-022-03658-5

Yu, X., Yang, L., Feng, Y., 2020. Comparative response of SOD in different plants against cadmium and drought stress at the molecular level. Applied Environmental Biotechnology, 5(1): 15-28.

https://doi.org/10.26789/AEB.2020.01.003

Zagorchev, L., Atanasova, A., Albanova, I., Traianova, A., Mladenov, P., Kouzmanova, M., Goltsev, V., Kalaji, H.M., Teofanova, D., 2021. Functional characterization of the photosynthetic machinery in Smicronix galls on the parasitic plant Cuscuta campestris by JIP-Test. Cells, 10(6): 1399.

https://doi.org/10.3390/cells10061399

Zhu, Q., Liu, X., Hao, T., Zeng, M., Shen, J., Zhang, F., Vries, W., 2020. Cropland acidification increases risk of yield losses and food insecurity in China. Environmental pollution, 256: 113145.

https://doi.org/10.1016/j.envpol.2019.113145

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DOI: https://doi.org/10.26789/AEB.2023.01.005

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