Abstract
In this research we report the significant effect of the floating water fern Azolla filiculoides on the elimination of hydrazine (N2H4) from water, which is a remarkable role for an aquatic plant. Hydrazine is a highly toxic compound for human health and biodiversity with wide industrial applications. In search of a practical way for hydrazine removal from an industrial wastewater, we studied the possible ability of certain aquatic lower plants to consume hydrazine. In greenhouse experiments, algal samples including Cladophora glomerata, Cosmarium sp. and Chlorella sp. did not show a significant effect on the rate of hydrazine elimination from water. However, A. filiculoides showed considerable growth when using hydrazine as the sole source of nitrogen. It was able to tolerate up to 4 mg/l hydrazine in the nutrient solution. During more than one month at the scale of 1/1000, Azolla removed hydrazine from boiler blowdown in the real conditions of a combined-cycle power plant. To our knowledge, this is the first observation of hydrazine consumption by a eukaryotic structure. Although we have discussed some possibilities, the exact mechanism of the process remains to be uncovered. On the other hand, considering the well-known abilities for bioremediation of a large number of contaminants from water, Azolla would be able to work as part of a cost effective system for remediation of hydrazine along with many other pollutants from different kinds of contaminated water. However, using Azolla in a hydrazine remediation system needs detailed feasibility studies to take various considerations into account.
Similar content being viewed by others
References
Al-Baldawi IB, Abdullah SRS, Anuar N, Abu Hasan H (2018) Phytotransformation of methylene blue from water using aquatic plant (Azolla pinnata). Environ Technol Innovation 11:15–22. https://doi.org/10.1016/j.eti.2018.03.009
Bansal S, Soni NK, Khandelwal CL, Sharma PD (2007) Kinetics and mechanism of visible light induced oxidation of hydrazine by peroxodisulphate in aqueous solution containing tris-(2,2-bipyridine) ruthenium(II). Indian J Chem 46A:1969–1971
Bark KM, Lee HS, Cho WH, Park HR (2008) Photochemical behavior of ammonia in aqueous suspension of TiO2. Bull Korean Chem Soc 29(4):869–872
Chekroun KB, Sanchez E, Baghour M (2014) The role of algae in bioremediation of organic pollutants. Int Res J Public Environ Health 1(2):19–32
Choudhary G, Iiansen H, Donkin S, Kirman C (1997) Toxicological profile for hydrezines. U.S. Department of Health and Human Services, Agency for Toxic Substances & Disease Registry, Georgia
Cohen MF, Williams J, Yamasaki H (2002) Biodegradation of diesel fuel by an Azolla-derived bacterial consortium. J Environ Sci Health 9:1593–1606. https://doi.org/10.1081/ESE-120015423
Dhir B (2013) Phytoremediation: role of aquatic plants in environmental clean-up. Springer, New Delhi
Forni C, Nicolai MA, D’Egidio MG (2001) Potential of the small aquatic plants Azolla and Lemna for nitrogenous compounds removal from wastewater. WIT Trans Ecol Environ 49:315–324. https://doi.org/10.2495/WP010301
Freitas OMM, Martins RJE, Delerue-Matos CM, Boaventura RA (2008) Removal of Cd(II), Zn(II) and Pb(II) from aqueous solutions by brown marine macro algae: kinetic modelling. J Hazard Mater 153(1):493–501. https://doi.org/10.1016/j.jhazmat.2007.08.081
Gogolashvili EL, Molgacheva IV, Isakov AA (2001) Detoxication of hydrazine in waste waters. Therm Eng 48(11):937–943
Golzary A, Tavakoli O, Rezaei Y, Karbasi AR (2018) Wastewater treatment by Azolla filiculoides (a study on color, odor, COD, nitrate, and phosphate removal). Pollution 4(1):69–76
Heck WW, Bloodworth ME, Clark WJ, Darling DR, Hoover W (1963) Environmental pollution by missile propellants. Wright-Patterson Air Force Base, Aerospace Medical Research Laboratory, Ohio
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. University of California, Berkeley
Hussner A (2010) NOBANIS—invasive alien species fact sheet—Azolla filiculoides. Online database of the European Network on invasive alien species—NOBANIS. Retrieved 18 september 2016 from www.nobanis.org
Ito O, Watanabe I (1983) The relationship between combined nitrogen uptakes and nitrogen fixation in Azolla–Anabaena symbiosis. New Phytol 95:647–654. https://doi.org/10.1111/j.1469-8137.1983.tb03528.x
Jampeetong A, Sripakdee T, Khamphaya T, Chairuangsri S (2016) The effects of nitrogen as NO3− and NH4+ on the growth and symbiont (Anabaena azollae) of Azolla pinnata R. Brown. CMU J Nat Sci 15(1):11–20
Kane DA, Williamson KJ (1983) Bacterial toxicity and metabolism of hydrazine fuels. Arch Environ Contam Toxicol 12:447–453. https://doi.org/10.1007/BF01057588
Kaplan D, Calvert HE, Peters GA (1986) The Azolla–Anabaena azollae relationship. Plant Physiol 80:884–890
Kollah B, Patra AK, Mohanty SR (2016) Aquatic microphylla Azolla: a perspective paradigm for sustainable agriculture, environment and global climate change. Environ Sci Pollut Res 23:4358–4369. https://doi.org/10.1007/s11356-015-5857-9
Kuch DJ (1996) Bioremediation of hydrazine: a literature review, AL/EQ-TR-1994-0055. Tyndall Air Force Base, Armstrong Laboratory, Forida
Lee YC, Chang SP (2011) The biosorption of heavy metals from aqueous solution by Spirogyra and Cladophora filamentous macroalgae. Bioresource Technol 102(9):5297–5304. https://doi.org/10.1016/j.biortech.2010.12.103
MacNaughton MG, Urda GA, Bowden SE (1978) Oxidation of hydrazine in aqueous solutions. Civil and Environmental Engineering Development Office, Environmental Sciences Research Division, Florida
McPhee W, Martin P (1994) Methods of catalytic photooxidation. US Patent, 5,324,438
Meeks JC, Steinberg NA, Enderlin CS, Joseph CM, Peters GA (1987) Azolla–Anabaena relationship XIII. Fixation of [13N]N2. Plant Physiol 84:883–886. https://doi.org/10.1104/pp.84.3.883
National Toxicology Program (2016) Reports on carcinogens: hydrazine and hydrazine sulfate. U.S. Department of Health and Human Services, National Toxicology Program. Retrieved 1 April 2017 from https://ntp.niehs.nih.gov/pubhealth/roc/index-1.html.
Negri M, Grund L (2015) Replacement of hydrazine: overview and first results of the H2020 project rheform. In: 6th European Conference for Aeronautics and Space Sciences, Dresden
Newton WE (2007) Physiology, biochemistry, and molecular biology of nitrogen fixation. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, New York, pp 109–129
Newton JW, Selke ES (1981) Assimilation of ammonia by the Azolla–Anabaena symbiosis. J Plant Nutr 3(5):803–811. https://doi.org/10.1080/01904168109362880
Norman JS, Friesen ML (2017) Complex N acquisition by soil diazotrophs: how the ability to release exoenzymes affects N fixation by terrestrial free-living diazotrophs. ISME J 11:315–326. https://doi.org/10.1038/ismej.2016.127
Oh JA, Park JH, Shin HS (2013) Sensitive determination of hydrazine in water by gas chromatography-mass spectrometry after derivatization with ortho-phthalaldehyde. Anal Chim Acta 769:79–83. https://doi.org/10.1016/j.aca.2013.01.036
Oh JA, Shin HS (2012) Determination of ortho-phthalaldehyde in water by high performance liquid chromatography and gas chromatography-mass spectrometry after hydrazine derivatization. J Chromatogr A 1247:99–103. https://doi.org/10.1016/j.chroma.2012.05.065
Op den Camp HJM, Jetten MSM, Strous M (2007) Anammox. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, New York, pp 245–262
Ou LT (1988) Degradation of monomethylhydrazine by two soil bacteria. Bull Environ Contam Toxicol 41:851–857. https://doi.org/10.1007/BF02021046
Ou LT (1987) Microbial degradation of hydrazine. Bull Environ Contam Toxicol 39:78–85. https://doi.org/10.1007/BF01691793
Prakash VAS, Krishna MPSM, Krishna VSGM (2012) Reuse, recycle and reduce of water from steam water system analyzer drain in thermal/gas based power plant. Int J Eng Sci Adv Technol 2(5):1251–1257
Priyadarshani I, Sahu D, Rath B (2011) Microalgal bioremediation:current practices and perspectives. J Biochem Technol 3(3):299–304
Rai AN, Bergman B, Rasmussen U (2002) Cyanobacteria in symbiosis. Kluwer, Dordrecht
Ranade VV, Bhandari VM (2014) Industrial wastewater treatment, recyclying, and reuse. Elsevier, Oxford
Ray TB, Peters GA, Toia RE, Mayne BC (1978) Azolla–Anabaena relationship VIII. Photosynthetic characterization of the association and individual partners. Plant Physiol 62:463–467. https://doi.org/10.1104/pp.64.5.791
Samrot AV, Thirunalasundari T (2012) Effect of Oscillatoria willei—a marine cyanobacterium on hydrazine induced toxicity. Malays J Microbiol 8(4):229–234
Sari A, Tuzen M (2008) Biosorption of cadmium(II) from aqueous solution by red algae (Ceramium virgatum): equilibrium, kinetic and thermodynamic studies. J Hazard Mater 157:448–454. https://doi.org/10.1016/j.jhazmat.2008.01.008
Schalk J, Oustad H, Kuenen JG, Jetten MSM (1998) The anaerobic oxidation of hydrazine: a novel reaction in microbial nitrogen metabolism. FEMS Microbiol Lett 158:61–67. https://doi.org/10.1111/j.1574-6968.1998.tb12801.x
Shi DJ, Hall DO (1988) The Azolla–Anabaena association: historical perspective, symbiosis and energy metabolism. Bot Rev 54(4):353–386. https://doi.org/10.1007/BF02858416
Slonim AR, Gisclard JB (1976) Hydrazine degradation in aquatic systems. Bull Environ Contam Toxicol 16(3):301–309. https://doi.org/10.1007/BF01685892
Soman D, Anitha V, Arora A (2018) Bioremediation of municipal sewage water with Azolla microphylla. Int J Adv Res 6(5):101–108
Sood A, Uniyal PL, Prasanna R, Ahluwalia AS (2012) Phytoremediation potential of aquatic macrophyte, Azolla. Ambio 41:122–137. https://doi.org/10.1007/s13280-011-0159-z
Stein LY, Klotz MG (2016) The nitrogen cycle. Curr Biol 26:R83–R101. https://doi.org/10.1016/j.cub.2015.12.021
Thiem CTL, Brown CJ, Kiel J, Holwitt ME, Obrien GJ (1997) The chemical and biochemical degradation of hydrazine, USAFA-TR-97-01. United States Air Force Academy, Colorado
Van Agteren MH, Keuning S, Janssen BJ (1998) Handbook on biodegradation and biological treatment of hazardous organic compounds. Kluwer, Dordrecht
Yatazawa M, Tomomatsu M, Hosoda N, Nunomi K (1980) Nitrogen fixation in Azolla-Anabaena symbiosis as affected by mineral nutrient status. Soil Sci Plant Nutr 26(3):415–426. https://doi.org/10.1080/00380768.1980.10431227
Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimani NR, McHenry MP (2016) Potential use of algae for heavy metal bioremediation, a critical review. J Environ Manage 181:817–831. https://doi.org/10.1016/j.jenvman.2016.06.059
Zimmerman WJ (1992) Ammonium uptake and excretion in Azolla–Anabaena symbiosis. Biol Fertil Soils 13:192–194. https://doi.org/10.1007/BF00336279
Acknowledgements
This study was funded by Kerman Regional Electric Company under contract no 93.41 with Shahid Bahonar University of Kerman and Kerman Combined-Cycle Power Plant. The research grant was received by J. Zolala. Authors are grateful to Dr. Sonia Aghighi for final reviewing of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Eimoori, R., Zolala, J., Pourmohiabadi, H. et al. Contribution of Azolla filiculoides to hydrazine elimination from water. Wetlands Ecol Manage 28, 439–447 (2020). https://doi.org/10.1007/s11273-020-09722-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11273-020-09722-3