Abstract
Cobalt is an essential trace metal and plays a pivotal role in the growth of all living organisms. The exposure of cobalt in the aquatic environment is ubiquitous via both natural and anthropogenic activities. The present study was carried out to investigate the accumulation response of macrophyte Hydrilla verticillata (L.f.) Royle towards the cobalt exposure at different concentrations (1, 25, 50, 75 and 100 µM) for seven days. The results showed that the cobalt accumulation increased in treated H. verticillata (L.f.) Royle with increase in concentration. The Bioconcentration factor (BCF) values were high in plants exposed to higher concentration of cobalt. Increase in growth (shoot length) and pigments (chlorophyll a, b and total chlorophyll) were detected at 25 µM cobalt concentration, whereas the growth and pigments were declined in 50, 75 and 100 µM. There was no significant difference in the carotenoid content between control and treated plant. Antioxidant enzymes (superoxide dismutase, catalase, and peroxidase) were increased at higher concentrations of cobalt. The results indicated that the decline in growth and pigments, and an increase in antioxidant enzyme activities, were triggered by the accumulation of cobalt in the plant. These observations suggest that H. verticillata (L.f.) Royle is well equipped to accumulate low concentration of cobalt in tissues to increase its growth and detoxify ROS generation. The BCF results indicate the efficiency of using H. verticillata (L.f.) Royle as a phytostabilizer.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdul-Basset R, Issa AA, Adam MS (1995) Chlorophyllase activity: effects of heavy metals and calcium. Photosynthetica 31:421–425
Aebi H (1984) Catalase in vitro. Methods Enzymol 26:105–121. https://doi.org/10.1016/s0076-6879(84)05016-3
Ali B, Hayat S, Hayat Q, Ahmad A (2010) Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). J Plant Interact 5:223–231. https://doi.org/10.1080/17429140903370584
Arnon DI (1949) Copper enzyme in isolated chloroplast polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Ashraf S, Ali Q, Ahmad Z, Ashraf S, Naeem H (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727. https://doi.org/10.1016/j.ecoenv.2019.02.068
Balabanova B, Stafilov T, Baceva K (2015) Bioavailability and bioaccumulation characterization of essential and heavy metals contents in R. acetosa, S. oleracea and U. dioica from copper polluted and referent areas. J Environ Health Sci Eng 13:2. https://doi.org/10.1186/s40201-015-0159-1
Bruland KW, Donat JR, Hutchins DA (1991) Interactive influences of bioactive trace metals on biological production in oceanic waters. Limnol Oceanogr 36:1555–1577. https://doi.org/10.4319/lo.1991.36.8.1555
Bunluesin S, Kruatrachue M, Pokethitiyook P, Upatham S, Lanza GR (2007) Batch and continuous packed column studies of cadmium biosorption by Hydrilla verticillata biomass. J Biosci Bioeng 103:509–513. https://doi.org/10.1263/jbb.103.509
Carvalho KM, McGettigan MJ, Martin DF (2001) GC/MS analysis of volatile organic selenium species produced during phytoremediation. J Environ Sci Health Part A 36(7):1403–1409. https://doi.org/10.1081/ESE-100104887
Ceyhun SB, Aksakal E, Ekinci D (2011) Influence of cobalt and zinc exposure on mRNA expression profiles of metallothionein and cytochrome P450 in rainbow trout. Biol Trace Elem Res 144:781–789. https://doi.org/10.1007/s12011-011-9068-z
Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74. https://doi.org/10.1016/s0269-7491(99)00238-9
Dixit S, Dhote S (2010) Evaluation of uptake rate of heavy metals by Eichhornia crassipes and Hydrilla verticillata. Environ Monit Assess 169:367–374. https://doi.org/10.1007/s10661-009-1179-z
Duman F, Leblebici Z, Aksoy A (2009) Growth and bioaccumulation characteristics of watercress (Nasturtium officinale R. BR.) exposed to cadmium, cobalt and chromium. Chem Speciat Bioavailab 21(4):257–265. https://doi.org/10.3184/095422909X12578511366924
Duraipandian M, Marisamy K, Periyanayagi G, Sevugaperumal R, Ganesh D, Ramasubramanian V (2016) Impact of cobalt on the growth, pigmental, some biochemical and enzymatic characteristics of Eleusine coracana (L.) Gaertin. American-Eurasian. J Toxicol Sci 8:115–119
Duxbury AC, Yentsch CS (1956) Plantkton pigment monograph. J Mar Res 15:92–101
Eid EM, Shaltout KH, Moghanm FS, Youssef MS, El-Mohsnawy E, Haroun SA (2019) Bioaccumulation and translocation of nine heavy metals by Eichhornia crassipes in Nile Delta, Egypt: perspectives for phytoremediation. Int J Phytoremediat 21:821–830. https://doi.org/10.1080/15226514.2019.1566885
Eid EM, Galal TM, Sewelam NA, Talha NI, Abdallah SM (2020) Phytoremediation of heavy metals by four aquatic macrophytes and their potential use as contamination indicators: a comparative assessment. Environ Sci Pollut Res: 1–14. https://doi.org/10.1007/s11356-020-07839-9
El-Sheekh MM, El-Naggar AH, Osman MEH, EL-Mazaly E (2003) Effect of cobalt on growth, pigments and photosynthetic electron transport in Monoraphidium minutum and Nitzchia perminuta. Braz J Plant Physiol 15:159–166. https://doi.org/10.1590/S1677-04202003000300005
Gadd GM, Griffiths AJ (1977) Microorganisms and heavy metal toxicity. Microb Ecol 4:303–317. https://doi.org/10.1007/BF02013274
Gal J, Hursthouse A, Tatner P, Stewart F, Welton R (2008) Cobalt and secondary poisoning in the terrestrial food chain: data review and research gaps to support risk assessment. Environ Int 34:821–838. https://doi.org/10.1016/j.envint.2007.10.006
Garcia A, Baquedano FJ, Navarro P, Castillo FJ (1999) Oxidative stress induced by copper in sunflower plants. Free Radic Res 31:45–50. https://doi.org/10.1080/10715769900301311
Gupta M, Chandra P (1996) Bioaccumulation and physiological changes in Hydrilla verticillata (L.f.) Royle in response to mercury. Bull Environ Contam Toxicol 56:319–326. https://doi.org/10.1007/s001289900047
Haller WT, Sutton DL (1975) Community structure and competition between Hydrilla and Vallisneria. Hyacinth Control J 13:48–50
Harguintegy CA, Fernández-Cirelli A, Pignata ML (2014) Heavy metal accumulation in leaves of aquatic plant Stuckenia filiformis and its relationship with sediment and water in the Suquía river (Argentina). Micro Chem J 114:111–118. https://doi.org/10.1016/j.microc.2013.12.010
Jaleel CA, Changxing Z, Jayakumar K, Iqbal M (2009) Low concentration of cobalt increase growth, biochemical constituents, mineral status and yield in Zea Mays. J Sci Res 1:128–137. https://doi.org/10.3329/jsr.v1i1.1226
Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. https://doi.org/10.1093/bmb/ldg032
Johri N, Jacquillet G, Unwin R (2010) Heavy metal poisoning: the effects of cadmium on the kidney. Biometals 23:783–792. https://doi.org/10.1007/s10534-010-9328-y
Kamal M, Ghaly AE, Mahmoud N, Cote R (2004) Phytoaccumulation of heavy metals by aquatic plants. Environ Int 24:1029–1039. https://doi.org/10.1016/S0160-4120(03)00091-6
Kumar JIN, Soni H, Kumar RN, Bhatt I (2008) Macrophytes in phytoremediation of heavy metal contaminated water and sediments in Pariyej community reserve, Gujarat, India. Turk J Fish Aquat Sci 8:193–200
Kumar D, Bharti SK, Anand S, Kumar N (2018) Bioaccumulation and biochemical responses of Vetiveria zizanioides grown under cadmium and copper stresses. Environ Sustain 1:133–139. https://doi.org/10.1007/s42398-018-0009-z
Kuyucak N, Volesky B (1989) Biosorbents for recovery of metals from industrial solutions. Biotechnol Lett 10:137–142. https://doi.org/10.1007/BF01024641
Langeland KA, Shilling DG, Carter JL, Laroche FB, Steward KK, Madiera PT (1992) Chromosome morphology and number in various populations of Hydrilla verticillata (L.f.) Royle. Aquat Bot 42:253–263. https://doi.org/10.1016/0304-3770(92)90026-F
Lauwerys R, Lison D (1994) Health risks associated with cobalt exposure - an overview. Sci Total Environ 150:1–6. https://doi.org/10.1016/0048-9697(94)90125-2
Lin H, Peng Y, Chen J, Liang L (2015) Effect of heavy metal stress on antioxidase enzymes. In: Proceedings of international conference on manufacturing science and engineering (ICMSE 2015), pp 871–876. https://doi.org/10.2991/icmse-15.2015.157
Lowry OH, Roenbrough NJ, Farr AL, Randal EJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Maehly AC, Chance B (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775. https://doi.org/10.1002/9780470110171$4ch14
Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
Miretzky P, Saralegui A, Cirelli FA (2004) Aquatic macrophytes potential for the simultaneous removal of heavy metals (Buenos Aires, Argentina). Chemosphere 57:997–1005. https://doi.org/10.1016/j.chemosphere.2004.07.024
Mishra VK, Tripathi B (2008) Concurrent removal and accumulation of heavy metals by the three aquatic macrophytes. Bioresour Technol 99:7091–7097. https://doi.org/10.1016/j.biortech.2008.01.002
Nagpal NK (2004) Technical report-water quality guideline for cobalt. Victoria (BC): water protection section, water, air and climate change branch, Ministry of water, land and air protection. Report No.: TD226.B7N33 2004. Contract No.:C20049601296
Nayek S, Gupta S, Saha R (2010) Effects of metal stress on biochemical response of some aquatic macrophytes growing along an industrial waste discharge channel. J Plant Interact 5(2):91–99. https://doi.org/10.1080/17429140903282904
Pandey N, Pathak GC, Pandey DK, Pandey R (2009) Heavy metals Co, Ni, Cu, Zn and Cd produce oxidative damage and evoke differential antioxidant responses in spinach. Braz J Plant Physiol 21:103–111. https://doi.org/10.1590/S1677-04202009000200003
Prajapati SK, Meravi N, Singh S (2012) Phytoremediation of chromium and cobalt using pistia stratiotes: A sustainable approach. Proc Int Acad Ecol Environ Sci 2(2):136
Radziemska M, Vaverková MD, Baryła A (2017) Phytostabilization-management strategy for stabilizing trace elements in contaminated soils. Int J Environ Res Public Health 14:958. https://doi.org/10.3390/ijerph14090958
Rai UN, Tripathi RD, Sinha S, Chandra P (1995) Chromium and cadmium bioaccumulation and toxicity in Hydrilla verticillata (L.f.) Royle and Chara corallina wildenow. J Environ Sci Health A Environ Sci Eng Toxicol 30:537–551. https://doi.org/10.1080/10934529509376216
Rai V, Vajpayee P, Mehratra S (2004) Effects of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169. https://doi.org/10.1016/j.plantsci.2004.06.016
Reed RH, Gadd GM (1989) Metal tolerance in eukaryotic and prokaryotic algae. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press Inc, Boca, pp 105–118
Reinardy HC, Syrett JR, Jeffree RA, Henry TB, Jha AN (2013) Cobalt-induced genotoxicity in male zebrafish (Danio rerio), with implications for reproduction and expression of DNA repair genes. Aquat Toxicol 126:224–230. https://doi.org/10.1016/j.aquatox.2012.11.007
Saleh HM, Bayoumi TA, Mahmoud HH, Aglan RF (2017) Uptake of cesium and cobalt radionuclides from simulated radioactive wastewater by Ludwigia stolonifera aquatic plant. Nucl Eng Des 315:194–199. https://doi.org/10.1016/j.nucengdes.2017.02.018
Sasmaz A, Obek E, Hasar H (2008) The accumulation of heavy metals in Typha latifolia L. Grown in a stream carrying secondary effluent. Ecol Eng 33:278–284. https://doi.org/10.1016/j.ecoleng.2008.05.006
Shalygo NV, Kolesnikova NV, Voronetskaya VV, Averina NG (1999) Effect of Mn2+, Fe2+, Co2+ and Ni2+ on chlorophyll accumulation and early stages of chlorophyll formation in greening barley seedling. Russ J Plant Physiol 46:496–501
Shearer JF, Michael JG, Dwilette GM (2007) Nutritional quality of Hydrilla verticillata (L.f.) Royle and its effects on a fungal pathogen Mycolepto discusterrestris (Gerd.) Ostazeski. Biol Control 41:175–183. https://doi.org/10.1016/j.biocontrol.2007.02.003
Shehata HS (2019) Using a phytoremediation approach to treat Egyptian watercourses with heavy metal contamination. Int J Environ Sci Technol 16:4437–4446. https://doi.org/10.1007/s13762-018-2031-1
Singh DB, Prasad G, Rupainwar DC (1996) Adsorption technique for the treatment of As (V) rich effluents. Colloids Surf A Physico Chem Eng Asp 111:49–56. https://doi.org/10.1016/0927-7757(95)03468-4
Singh AL, Jat RS, Chaudhari V, Bariya H, Sharma SJ (2010) Toxicities and tolerance of mineral elements boron, cobalt, molybdenum and nickel in crop plants. Plant nutrition and abiotic stress tolerance II. Plant Stress 4:31–56
Singh A, Kumar CS, Agarwal A (2013) Effect of lead and cadmium on aquatic plant Hydrilla verticillata. J Environ Biol 34:1027–1031
Singh N, Kaur M, Katnoria JK (2017) Analysis on bioaccumulation of metals in aquatic environment of Beas river basin: a case study from Kanjli wetland. Geo Health 1:93–105. https://doi.org/10.1002/2017GH000062
Sinha S, Pandey K (2003) Nickel-induced toxic effects and bioaccumulation in the submerged plant, Hydrilla verticillata (L.f.) Royle under repeated metal exposure. Bull Environ Contam Toxicol 71:1175–1183. https://doi.org/10.1007/s00128-003-8896-8
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Gupta DK (2006) Copper-induced oxidative stress and responses of antioxidants and phytochelatins in Hydrilla verticillata (L.f.) Royle. Aquat Toxicol 80:405–415. https://doi.org/10.1016/j.aquatox.2006.10.006
Stroinski A (1994) Cadmium signaling in plant cell. Biol Plantarum 36:299
Suganthi P, Soundarya N, Stalin A, Nedunchezhiyan S (2015) Toxicological effect of cobalt chloride on freshwater fish Oreochromis mossambicus. Int J Sci Appl Res 1:331–340
SwaminathanK, Arjunan S, Gurusamy R (1990) Effect of glucose factory effluents on the seed germination and seedling development of groundnut (Arachis hypogeal L.). In: Dalela RC, Muley DV, Panday SN, Deshmukh PB, Selavanayagam M (eds) Environmental impact on biosystems. The Academy of Environmental Biology, Muzaffarnagar (India), pp 81–87
Tewari RK, Kumar P, Sharma PN, Bisht SS (2002) Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 162:381–388. https://doi.org/10.1016/S0168-9452(01)00578-7
Vymazal J, Kropfelova L (2008) Wastewater treatment in constructed wetlands with horizontal sub-surface flow. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8580-2
Wang S, Jin X, Zhao H, Wu F (2008) Phosphate biosorption characteristics of a submerged macrophyte Hydrilla verticillata. Aquat Bot 89:23–26. https://doi.org/10.1016/j.aquabot.2008.01.006
Wolverton BC, McDonald RC (1975) Water hyacinths and alligator weeds for removal of lead and mercury from polluted waters. NASA Technical Memorandum X-72723, National Space Technological Laboratories, Bay St. Louis
Xue PY, Li GX, Liu WJ, Yan CZ (2010) Copper uptake and translocation in a submerged aquatic plant Hydrilla verticillata (L.f.). Royle Chemosphere 81:1098–1103. https://doi.org/10.1016/j.chemosphere.2010.09.023
Yan Y, Jian-ping L, Zhang XH (2008) Response of Hyperaccumulator Leersia hexandra Swart to chromium-induced oxidative stress. Environ Ecol 17:1476–1482
Zeeshan M, Murugadas A, Ghaskadbi S, Ramaswamy BR, Akbarsha MA (2017) Ecotoxicological assessment of cobalt using hydra model: ROS, oxidative stress, DNA damage, cell cycle arrest, and apoptosis as mechanisms of toxicity. Environ Pollut 224:54–69. https://doi.org/10.1016/j.envpol.2016.12.042
Zhang H, Zhang L, Li J, Chen M, An R (2020) Comparative study on the bioaccumulation of lead, cadmium and nickel and their toxic effects on the growth and enzyme defence strategies of a heavy metal accumulator, Hydrilla verticillata (L.f.) Royle. Environ Sci Pollut Res (2020). https://doi.org/10.1007/s11356-019-06968-0
Acknowledgements
The authors thank University Grants Commission - Special Assistance Programme - Departmental Research Support (UGC-SAP-DRS-II) (F.3-9/2013[SAP-II]), Department of Science and Technology Promotion of University Research and Scientific Excellence (DST PURSE Phase - II) (Ref. No. SR/PURSE PHASE 2/16(G) /& 16(C) Date. 21.02.2017) and Department of Science and Technology Fund for Improvement of S & T Infrastructure in Higher Educational Institutions (DST FIST) Level - I (stage-II) (Ref. No. SR/FST/LSI-647/2015(C) Date.11.08.2016) for the instrumentation support to Department of Animal Science, Bharathidasan University, Tiruchirappalli.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Rights and permissions
About this article
Cite this article
Sridhar, A., Khader, P.A. & Ramasamy, T. Assessment of cobalt accumulation effect on growth and antioxidant responses in aquatic macrophyte Hydrilla verticillata (L.f.) Royle. Biologia 75, 2001–2008 (2020). https://doi.org/10.2478/s11756-020-00497-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-020-00497-9