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Residual pollutants in treated pulp paper mill wastewater and their phytotoxicity and cytotoxicity in Allium cepa

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Abstract

Discharged pulp and paper mill wastewater (PPMW) were collected near M/s K. R. pulp and papers Limited, Shahjahanpur, India. Chemical analysis of the wastewater showed high BOD (3653–4180 mg L−1) and COD (17,890–19100 mg L−1) values from two different sampling sites. The levels of total phenol were in the range of 389–432 mg L−1; nitrogen (125–234 mg L−1), sulfate (1926–2098 mg L−1), chloride (3.12–5.43 mg L−1) and lignin (38,950–39,000 mg L−1) along with various heavy metals (Fe, 87–79; Zn, 34–22; Cu, 3.28–2.57; Cd, 1.90–0.36; Ni, 6–5, and Pb, 41.23–36.54 mg L−1) were above the permissible limits recommended by the CPCB and the USEPA. The BOD/COD ratio was  < 0.2 which indicated very low biodegradability of the organic matters present in the effluent. The organometallic complex generated from the pulp and paper industry persists in the environment and might be toxic to aquatic organisms. The organic polymers, lignin, metals and ions present in the PPMW were characterized using SEM, EDAX, FTIR, and UV–VIS spectroscopy. The major pollutants detected in the discharged PPMW included nonacosane, heptacosane, octadecanoic acid, hexadecane, and 6-benzamide- 3- [2- [1-(phenylmethyl)-4-piperidinyl] ethyl]-1, 2-benzisoxazole, as well as a group of plant fatty acids classified as EDCs, and mutagenic pollutants. The cytotoxic and androgenic properties of these complex organics were examined. The seed germination test with Phaseolus mungo and cytotoxicity test with Allium cepa showed that at > 20% concentration of PPMW, α-amylase production was inhibited and chromosomal segregation at metaphase and anaphase during cell division was disturbed, which resulted in c-mitosis, sticky chromosomes, and laggard chromosomes. In addition, SEM of the root of A. cepa showed fissures and fractured tissues of the root cap, probably due to the inhibition of auxins that were responsible for root cap formation. The findings indicated A. cepa as a good test model for examining the DNA damage and cytotoxicity by PPMW, and the discharged effluent should be treated at a tertiary stage for environmental protection.

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References

  • Afroz, Z., & Singh, A. (2014). Impact of pulp and paper mill effluent on water quality of river Aami and its effect on aquatic life (fish). Global Journal Pharmacol, 8(2), 140–149.

    CAS  Google Scholar 

  • Afshan, S., Ali, S., Ameen, U. S., Farid, M., Bharwana, S. A., Hannan, F., et al. (2014). Effect of different heavy metal pollution on fish. Research Journal of Chemical and Environmental Sciences, 2(1), 74–79.

    CAS  Google Scholar 

  • Ahmad, I., Maria, V. L., Oliveira, M., Pacheco, M., & Santos, M. A. (2006). Oxidative stress and genotoxic effects in gill and kidney of Anguilla anguilla L. exposed to chromium with or without pre-exposure to β-naphthoflavone. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 608(1), 16–28.

    Article  CAS  Google Scholar 

  • Ahmed, E. M. (2015). Hydrogel: Preparation, characterization, and applications: A review. Journal of Advanced Research, 6(2), 105–121.

    Article  CAS  Google Scholar 

  • Aina, R., Palin, L., & Citterio, S. (2006). Molecular evidence for benzo [a] pyrene and naphthalene genotoxicity in Trifolium repens L. Chemosphere, 65(4), 666–673.

    Article  CAS  Google Scholar 

  • Ali, M., & Sreekrishnan, T. R. (2001). Aquatic toxicity from pulp and paper mill effluents: A review. Advances in Environmental Research, 5(2), 175–196.

    Article  CAS  Google Scholar 

  • APHA (American Public Health Association): Standard Method for Examination of Water and Wastewater, 22nd ed. Washington, DC. (2012).

  • Batista, A. H., Melo, V. F., Gilkes, R., & Roberts, M. (2018). Identification of heavy metals in crystals of sand and silt fractions of soils by scanning electron microscopy (SEM-EDS/WD-EPMA). Revista Brasileira de Ciência do Solo42.

  • Bharagava, R. N., & Chandra, R. (2010). Effect of bacteria treated and untreated post-methanated distillery effluent (PMDE) on seed germination, seedling growth, and amylase activity in Phaseolus mungo L. Journal of Hazardous Materials, 180(1–3), 730–734.

    Article  CAS  Google Scholar 

  • Central pulp paper research Institute (CPPRI) Annual report (2016–17) Saharanpur (U.P.) India.

  • Chandra, R., & Abhishek, A. (2011). Bacterial decolorization of black liquor in axenic and mixed condition and characterization of metabolites. Biodegradation, 22(3), 603–611.

    Article  CAS  Google Scholar 

  • Chandra, R., & Kumar, V. (2017). Detection of androgenic-mutagenic compounds and potential autochthonous bacterial communities during in situ bioremediation of post-methanated distillery sludge. Frontiers in microbiology, 8, 887.

    Article  Google Scholar 

  • Chandra, R., Raj, A., Yadav, S., & Patel, D. K. (2009). Reduction of pollutants in pulp paper mill effluent treated by PCP-degrading bacterial strains. Environmental Monitoring and Assessment, 155(1–4), 1.

    Article  CAS  Google Scholar 

  • Chandra, R., Sharma, P., Yadav, S., & Tripathi, S. (2018). Biodegradation of endocrine-disrupting chemicals and residual organic pollutants of pulp and paper mill effluent by biostimulation. Frontiers in Microbiology, 9, 960.

    Article  Google Scholar 

  • Chandra, R., & Singh, R. (2012). Decolourisation and detoxification of rayon grade pulp paper mill effluent by mixed bacterial culture isolated from pulp paper mill effluent polluted site. Biochemical Engineering Journal, 61, 49–58.

    Article  CAS  Google Scholar 

  • Chandra, R., Singh, S., & Raj, A. (2006). Seasonal bacteriological analysis of Gola river water contaminated with pulp paper mill waste in Uttaranchal, India. Environmental Monitoring and Assessment, 118(1–3), 393–406.

    Article  CAS  Google Scholar 

  • Chandra, R., Singh, R., & Yadav, S. (2012). Effect of bacterial inoculums ratio in mixed culture for decolorization and detoxification of pulp paper mill effluent. Journal of Chemical Technology and Biotechnology, 87(3), 436–444.

    Article  CAS  Google Scholar 

  • Chandra, R., & Yadav, S. (2010). The potential of Typha angustifolia for phytoremediation of heavy metals from an aqueous solution of phenol and melanoidin. Ecological Engineering, 36(10), 1277–1284.

    Article  Google Scholar 

  • Chandra, R., Yadav, S., & Yadav, S. (2017). Phytoextraction potential of heavy metals by native wetland plants growing on chlorolignin containing sludge of pulp and paper industry. Ecological Engineering, 98, 134–145.

    Article  Google Scholar 

  • Chiang, G., Barra, R., Díaz-Jaramillo, M., Rivas, M., Bahamonde, P., & Munkittrick, K. R. (2015). Estrogenicity and intersex in juvenile rainbow trout (Oncorhynchus mykiss) exposed to Pine/Eucalyptus pulp and paper production effluent in Chile. Aquatic Toxicology, 164, 126–134.

    Article  CAS  Google Scholar 

  • Chowdhury, U. K., Biswas, B. K., Chowdhury, T. R., Samanta, G., Mandal, B. K., Basu, G. C., et al. (2000). Groundwater arsenic contamination in Bangladesh and West Bengal, India. Environmental Health Perspectives, 108(5), 393–397.

    Article  CAS  Google Scholar 

  • de Sousa Andrade, L. N., De Lima, T. M., Curi, R., & de Lauro Castrucci, A. M. (2005). Toxicity of fatty acids on murine and human melanoma cell lines. Toxicology in Vitro, 19(4), 553–560.

    Article  Google Scholar 

  • Deepali, K. K., Gangwar, R., & Joshi, B. D. (2009). Comparative study of Physico-chemical properties of effluent from tannery industries. Indian Journal of Environmental Sciences, 3(2), 49–152.

    Google Scholar 

  • EPA (2012) seedling emergence and seedling growth emergence and growth test PPT-21.

  • Farag, A. M., May, T., Marty, G. D., Easton, M., Harper, D. D., Little, E. E., et al. (2006). The effect of chronic chromium exposure on the health of Chinook salmon (Oncorhynchus tshawytscha). Aquatic Toxicology, 76(3–4), 246–257.

    Article  CAS  Google Scholar 

  • Fendri, I., Ben Saad, R., Khemakhem, B., Ben Halima, N., Gdoura, R., & Abdelkafi, S. (2013). Effect of treated and untreated domestic wastewater on seed germination, seedling growth and amylase and lipase activities in Avena sativa L. Journal of the Science of Food and Agriculture, 93(7), 1568–1574.

    Article  CAS  Google Scholar 

  • Firbas, P., & Amon, T. (2013). Allium chromosome aberration test for evaluation effect of cleaning municipal water with Constructed Wetland (CW) in Sveti Tomaž, Slovenia. Journal of Bioremediation and Biodegradation, 4(4), 189.

    Article  Google Scholar 

  • Firbas, P., & Amon, T. (2014). Chromosome damage studies in the onion plant Allium cepa L. Caryologia, 67(1), 25–35.

    Article  Google Scholar 

  • Gauthier, F., & Archibald, F. (2001). The ecology of “fecal indicator” bacteria commonly found in pulp and paper mill water systems. Water Research, 35(9), 2207–2218.

    Article  CAS  Google Scholar 

  • González, T., Terrón, M. C., Yagüe, S., Zapico, E., Galletti, G. C., & González, A. E. (2000). Pyrolysis/gas chromatography/mass spectrometry monitoring of fungal‐biotreated distillery wastewater using Trametes sp. I‐62 (CECT 20197). Rapid Communications in Mass.

  • Hankin, L., & Kolattukudy, P. E. (1968). Metabolism of a plant wax paraffin (n-nonacosane) by a soil bacterium (Micrococcus cerificans). Microbiology, 51(3), 457–463.

    CAS  Google Scholar 

  • Haq, I., Kumar, S., Raj, A., Lohani, M., & Satyanarayana, G. N. V. (2017). Genotoxicity assessment of pulp and paper mill effluent before and after bacterial degradation using the Allium cepa test. Chemosphere, 169, 642–650.

    Article  CAS  Google Scholar 

  • Hou, L. P., Yang, Y., Shu, H., Ying, G. G., Zhao, J. L., Fang, G. Z., et al. (2018). Masculinization and reproductive effects in western mosquitofish (Gambusia affinis) after long-term exposure to androstenedione. Ecotoxicology and Environmental Safety, 147, 509–515.

    Article  CAS  Google Scholar 

  • Huang, M., Qi, F., Shi, X., & Hu, H. (2015). COD fractionation and toxicity of pulp and paper mill wastewaters in a tertiary process. Desalination and Water Treatment, 56(3), 615–621.

    Article  CAS  Google Scholar 

  • Ilić, S. Z., Mirecki, N., Trajković, R., Kapoulas, N., Milenković, L., & Šunić, L. (2015). Effect of Pb on germination of different seed and his translocation in bean seed tissues during sprouting. Fresenius Environmental Bulletin, 24(2A), 670–675.

    Google Scholar 

  • Iqbal, H. M. N., Kyazze, G., & Keshavarz, T. (2013). Advances in the valorization of lignocellulosic materials by biotechnology: An overview. BioResources, 8(2), 3157–3176.

    Article  Google Scholar 

  • Ivanov, V. B., Bystrova, E. I., & Seregin, I. V. (2003). Comparative impacts of heavy metals on root growth as related to their specificity and selectivity. Russian Journal of Plant Physiology, 50(3), 398–406.

    Article  CAS  Google Scholar 

  • Kågedal, K., Bironaite, D., & Öllinger, K. (1999). Anthraquinone cytotoxicity and apoptosis in primary cultures of rat hepatocytes. Free Radical Research, 31(5), 419–428.

    Article  Google Scholar 

  • Karrasch, B., Parra, O., Cid, H., Mehrens, M., Pacheco, P., Urrutia, R., et al. (2006). Effects of pulp and paper mill effluents on the microplankton and microbial self-purification capabilities of the Biobio River, Chile. Science of the Total Environment, 359(1–3), 194–208.

    Article  CAS  Google Scholar 

  • Kaushik, G., Gopal, M., & Thakur, I. S. (2010). Evaluation of performance and community dynamics of microorganisms during treatment of distillery spent wash in a three-stage bioreactor. Bioresource Technology, 101(12), 4296–4305.

    Article  CAS  Google Scholar 

  • Khan, S. R., Finlayson, B., & Hackett, R. (1984). Renal papillary changes in patient with calcium oxalate lithiasis. Urology, 23(2), 194–199.

    Article  CAS  Google Scholar 

  • Kumar, V., Chopra, A. K., Kumar, S., Singh, J., & Thakur, R. K. (2015). Effects of pulp and paper mill effluent disposal on soil characteristics in the vicinity of Uttaranchal Pulp and Paper Mill, Haridwar (Uttarakhand), India. International Journal of Agriculture Science and Research, 4, 117–125.

    Google Scholar 

  • Lacorte, S., Latorre, A., Barcelo, D., Rigol, A., Malmqvist, A., & Welander, T. (2003). Organic compounds in paper-mill process waters and effluents. TrAC Trends in Analytical Chemistry, 22(10), 725–737.

    Article  CAS  Google Scholar 

  • Ladwani, K. D., Ladwani, K. D., Ramteke, D. S., & Deo, S. (2016). Detection and identification of organic compounds in wastewater of final effluent treatment plant by FTIR and GC-MS. Journal of Advanced Chemical Sciences, 246–247.

  • Leach, J. M., & Thakore, A. N. (1978, January). Compounds toxic to fish in pulp mill waste streams. In Eighth international conference on water pollution research (pp. 787–798). Pergamon.

  • Leme, D. M., & Marin-Morales, M. A. (2009). Allium cepa test in environmental monitoring: A review on its application. Mutation Research/Reviews in Mutation Research, 682(1), 71–81.

    Article  CAS  Google Scholar 

  • Lindholm-Lehto, P. C., Knuutinen, J. S., Ahkola, H. S., & Herve, S. H. (2015). Refractory organic pollutants and toxicity in pulp and paper mill wastewaters. Environmental Science and Pollution Research, 22(9), 6473–6499.

    Article  CAS  Google Scholar 

  • Liu, X., Zhu, H., Qin, C., Zhou, J., Zhao, J. R., & Wang, S. (2013). Adsorption of heavy metal ion from aqueous single metal solution by aminated epoxy-lignin. BioResources, 8(2), 2257–2269.

    Article  CAS  Google Scholar 

  • Madan, S., Sachan, P., & Singh, U. (2018). A review on bioremediation of pulp and paper mill effluent –An alternative to conventional remedial technologies. Journal of Applied and Natural Science, 10(1), 367–374.

    Article  CAS  Google Scholar 

  • McMartin, D. W., Peru, K. M., Headley, J. V., Winkler, M., & Gillies, J. A. (2002). Evaluation of liquid chromatography-negative ion electro spray mass spectrometry for the determination of selected resin acids in river water. Journal of Chromatography A, 952(1–2), 289–293.

    Article  CAS  Google Scholar 

  • Müller, J. B., Melegari, S. P., Perreault, F., & Matias, W. G. (2019). Comparative assessment of acute and chronic ecotoxicity of water soluble fractions of diesel and biodiesel on Daphnia magna and Aliivibrio fischeri. Chemosphere, 221, 640–646.

    Article  Google Scholar 

  • Nefic, H., Musanovic, J., Metovic, A., & Kurteshi, K. (2013). Chromosomal and nuclear alterations in root tip cells of Allium cepa L. induced by alprazolam. Medical Archives, 67(6), 388.

    Article  Google Scholar 

  • Nurmesniemi, H., Pöykiö, R., Perämäki, P., & Kuokkanen, T. (2005). The use of a sequential leaching procedure for heavy metal fractionation in green liquor dregs from a causticizing process at a pulp mill. Chemosphere, 61(10), 1475–1484.

    Article  CAS  Google Scholar 

  • OECD. (2006). Terrestrial plant test: Seedling emergence and seedling growth test. OECD-Organization for Economic Cooperation and Development, Paris, 208, 6.

    Google Scholar 

  • Ojunga, S., Masese, F. O., Manyala, J. O., Etiégni, L., Onkware, A. O., Senelwa, K., et al. (2010). Impact of a kraft pulp and paper mill effluent on phytoplankton and macroinvertebrates in River Nzoia, Kenya. Water Quality Research Journal, 45(2), 235–250.

    Article  CAS  Google Scholar 

  • Ott, L. (1984). Introduction to the analysis of variance. An introduction to statistical methods and data analysis (pp. 325–336).

  • Peng, W. X., & Wu, & Y. Q. (2008). Py-GC/MS analysis on benzene/ethanol extractives of Eucalyptus camaldulensis wood meal in pulping wastewater from South China. In Proceedings of 2008 Conference on the Regional Economy and Sustainable Development.

  • Pokhrel, D., & Viraraghavan, T. (2004). Treatment of pulp and paper mill wastewater—a review. Science of the Total Environment, 333(1–3), 37–58.

    Article  CAS  Google Scholar 

  • Reddy, P. M., & Rao, N. S. (2001). Effects of industrial effluents on the groundwater regime in Visakhapatnam. Pollution Research, 20(3), 383–386.

    CAS  Google Scholar 

  • Réveillé, V., Mansuy, L., Jardé, É., & Garnier-Sillam, É. (2003). Characterization of sewage sludge-derived organic matter: Lipids and humic acids. Organic Geochemistry, 34(4), 615–627.

    Article  Google Scholar 

  • Savant, D. V., Abdul-Rahman, R., & Ranade, D. R. (2006). Anaerobic degradation of adsorbable organic halides (AOX) from pulp and paper industry wastewater. Bioresource Technology, 97(9), 1092–1104.

    Article  CAS  Google Scholar 

  • Sepulveda, M. S., Johnson, W. E., Higman, J. C., Denslow, N. D., Schoeb, T. R., & Gross, T. S. (2002). Evaluation of biomarkers of reproductive function and potential contaminant effects in Florida largemouth bass (Micropterus salmoides floridanus) sampled from the St. Johns River. Science of the Total Environment, 289, 133–144.

    Article  CAS  Google Scholar 

  • Shaymurat, T., Gu, J., Xu, C., Yang, Z., Zhao, Q., Liu, Y., et al. (2012). Phytotoxic and genotoxic effects of ZnO nanoparticles on garlic (Allium sativum L.): A morphological study. Nanotoxicology, 6(3), 241–248.

    Article  CAS  Google Scholar 

  • Singh, A. K., & Chandra, R. (2019). Pollutants released from the pulp paper industry: Aquatic toxicity and their health hazards. Aquatic Toxicology, 211, 202–2016.

    Article  CAS  Google Scholar 

  • Singh, V. K., Kavita, K., Prabhakaran, R., & Jha, B. (2013). Cis-9-octadecenoic acid from the rhizospheric bacterium Stenotrophomonas maltophilia BJ01 shows quorum quenching and anti-biofilm activities. Biofouling, 29(7), 855–867.

    Article  CAS  Google Scholar 

  • Slavin, Y. N., Asnis, J., Häfeli, U. O., & Bach, H. (2017). Metal nanoparticles: Understanding the mechanisms behind the antibacterial activity. Journal of Nanobiotechnology, 15(1), 65.

    Article  Google Scholar 

  • Smith, A. H., Lingas, E. O., & Rahman, M. (2000). Contamination of drinking-water by arsenic in Bangladesh: A public health emergency. Bulletin of the World Health Organization, 78, 1093–1103.

    CAS  Google Scholar 

  • Suntio, L. R., Shiu, W. Y., & Mackay, D. (1988). A review of the nature and properties of chemicals present in pulp mill effluents. Chemosphere, 17(7), 1249–1290.

    Article  CAS  Google Scholar 

  • Taylor, C. D., Smith, S. O., & Gagosian, R. B. (1981). Use of microbial enrichment for the study of the anaerobic degradation of cholesterol. Geochimica et Cosmochimica Acta, 45(11), 2161–2168.

    Article  CAS  Google Scholar 

  • USEPA (2002) the environment protection rules, 3A, Schedule-II, III. U.S. Environmental Protection Agency, Office of research and development, Cincinnati.

  • USEPA, U.S. Environmental Protection Agency (2012). Endocrine Disruptor Screening Program, Universe of Chemicals for Potential Endocrine Disruptor Screening and Testing, Jointly developed by the Office of Chemical Safety & Pollution Prevention, the Office of Water and the Office of Research and Development (pp 1–176).

  • Verma, K., Shekhawat, G. S., Sharma, A., Mehta, S. K., & Sharma, V. (2008). Cadmium-induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3–4 leaf stage plants of Brassica juncea (L.) czern. Plant Cell Reports, 27(7), 1261–1269.

    Article  CAS  Google Scholar 

  • Wong, M. H., & Bradshaw, A. D. (1982). A comparison of the toxicity of heavy metals, using root elongation of ryegrass, Lolium perenne. New Phytologist, 91(2), 255–261.

    Article  CAS  Google Scholar 

  • Yadav, S., & Chandra, R. (2018). Detection and assessment of the phytotoxicity of residual organic pollutants in sediment contaminated with pulp and paper mill effluent. Environmental Monitoring and Assessment, 190(10), 581.

    Article  Google Scholar 

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Acknowledgements

This work is financially supported by DBT, New Delhi, India vide letter no. BT/PR18896/BCE/8/1372/2016 Dated 28.3.2018 Govt. of India New Delhi. Instrumentation facilities for Scanning Electron Microscopy (SEM) from USIC, BBAU Lucknow, and Uttar Pradesh, India are gratefully acknowledged. This work formed part of the Ph.D. program of Ms. Pooja Sharma.

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Sharma, P., Purchase, D. & Chandra, R. Residual pollutants in treated pulp paper mill wastewater and their phytotoxicity and cytotoxicity in Allium cepa. Environ Geochem Health 43, 2143–2164 (2021). https://doi.org/10.1007/s10653-020-00730-z

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