Rapid ecotoxicological tests using bioassay systems - a review
DOI:
https://doi.org/10.54987/jobimb.v4i1.286Keywords:
Ecotoxicological tests, pollution, metal, bioassay, bacteriaAbstract
 The rise in pollution cases globally is expected to increase in line with industrialization. Monitoring activities for pollutants have been hampered by the astronomical costs of instrumental-based approach. This has resulted in the intense research on low cost biomonitoring systems using enzymes, organisms including microorganisms. Only positive samples are sent for instrumental analysis; dramatically cutting the cost of instrumental analysis. This review attempts to outline and give due recognition to several selected bioassay systems that have been tested for their applicability using polluted water samples as a routine first line-of-defense. This includes small aquatic organisms-based assays, enzymes especially proteases and bacterial-based systems using respiratory dye or luminescence systems as a method for toxicant detection.
References
Rieger PG, Meier HM, Gerle M, Vogt U, Groth T, Knackmuss HJ. Xenobiotics in the environment: present and future strategies to obviate the problem of biological persistence. J Biotechnol. 2002;94(1):101–123.
Isenberg DL, Bulich A. Environmental monitoring: use of luminescent bacteria. Chem Saf. 1994;211–226.
Cormier MJ, Totter JR. Bioluminescence. Enzymic aspects. Photophysiology. 1968;4:315–53.
Warne M, Boyd E, Meharg A, Osborn D, Killham K, Lindon J, et al. Quantitative structure-toxicity relationships for halobenzenes in two species of bioluminescent bacteria, Pseudomonas fluorescens and Vibrio fischeri, using an atom-centered semi-empirical molecular-orbital based model. SAR QSAR Environ Res. 1999;10(1):17–38.
Reddy VR, Behera B. Impact of water pollution on rural communities: An economic analysis. Ecol Econ. 2006;58(3):520–37.
Shukor Y, Baharom NA, Rahman FA, Abdullah MP, Shamaan NA, Syed MA. Development of a heavy metals enzymatic-based assay using papain. Anal Chim Acta. 2006;566(2):283–9.
Zheng L, Liu G, Chou CL. The distribution, occurrence and environmental effect of mercury in Chinese coals. Sci Total Environ. 2007;384(1–3):374–83.
Harada M. Congenital Minamata disease: intrauterine methylmercury poisoning. Teratology. 1978;18(2):285–8.
Takeuchi T, Morikawa N, Matsumoto H, Shiraishi Y. A pathological study of Minamata disease in Japan. Acta Neuropathol (Berl). 1962;2(1):40–57.
Klumpp DW, Humphrey C, Huasheng H, Tao F. Toxic contaminants and their biological effects in coastal waters of Xiamen, China.:: II. Biomarkers and embryo malformation rates as indicators of pollution stress in fish. Mar Pollut Bull. 2002;44(8):761–9.
Shi J, Ip C, Zhang G, Jiang G, Li X. Mercury profiles in sediments of the Pearl River Estuary and the surrounding coastal area of South China. Environ Pollut. 2010;158(5):1974–9.
Verlecar XN, Desai SR, Sarkar A, Dalal SG. Biological indicators in relation to coastal pollution along Karnataka coast, India. Water Res. 2006;40(17):3304–12.
Clark A, Turner T, Dorothy KP, Goutham J, Kalavati C, Rajanna B. Health hazards due to pollution of waters along the coast of Visakhapatnam, east coast of India. Ecotoxicol Environ Saf. 2003;56(3):390–7.
Abdullah AR. Environmental pollution in Malaysia: trends and prospects. TrAC Trends Anal Chem. 1995;14(5):191–8.
Ibrahim M. Persistent Organic Pollutants in Malaysia. Dev Environ Sci. 2007;7:629–55.
DOE. Malaysia Environmental Quality Report 2014. Department of Environment, Ministry of Natural Resources and Environment, Malaysia; 2015.
Al-Shami SA, Md Rawi CS, Ahmad AH, Abdul Hamid S, Mohd Nor SA. Influence of agricultural, industrial, and anthropogenic stresses on the distribution and diversity of macroinvertebrates in Juru River Basin, Penang, Malaysia. Ecotoxicol Environ Saf. 2011;74(5):1195–202.
Lim PE, Kiu MY. Determination and speciation of heavy metals in sediments of the Juru River, Penang, Malaysia. Environ Monit Assess. 1995;35(2):85–95.
Halmi MIE, Jirangon H, Johari WLW, Abdul Rachman AR, Shukor MY, Syed MA. Comparison of Microtox and Xenoassay light as a near real time river monitoring assay for heavy metals. Sci World J. 2014;2014.
Al-Shami SA, Rawi CS., HassanAhmad A, Nor SA. Distribution of Chironomidae (Insecta: Diptera) in polluted rivers of the Juru River Basin, Penang, Malaysia. J Environ Sci. 2010;22(11):1718–27.
Ku Ahamad KE, Halmi MIE, Shukor MY, Wasoh MH, Abdul Rachman AR, Sabullah MK, et al. Characterization of a diesel-degrading strain isolated from a local hydrocarbon-contaminated site. J Environ Bioremediation Toxicol. 2013;1(1):1–8.
AbdEl-Mongy MA, Shukor MS, Hussein S, Ling APK, Shamaan NA, Shukor MY. Isolation and characterization of a molybdenum-reducing, phenol- and catechol-degrading Pseudomonas putida strain amr-12 in soils from Egypt. Sci Study Res Chem Chem Eng Biotechnol Food Ind. 2015;16(4):353–69.
Duffus JHWHG., Worth HG. Toxicology and the environment: An IUPAC teaching program for chemists. Pure Appl Chem. 2006;78(11):2043–50.
Silva AL., Barrocas PR., Jacob SC, Moreira JC. Dietary intake and health effects of selected toxic elements. Braz J Plant Physiol. 2005;17(1):79–93.
Burton Jr GA. Assessing the toxicity of freshwater sediments. Environ Toxicol Chem. 1991;10(12):1585–627.
Freshney I. Application of cell cultures to toxicology. Cell Biol Toxicol. 2001;17(4):213–30.
Aidil MS, Sabullah MK, Halmi MIE, Sulaiman R, Shukor MS, Shukor MY, et al. Assay for heavy metals using an inhibitive assay based on the acetylcholinesterase from Pangasius hypophthalmus (Sauvage, 1878). Fresenius Environ Bull. 2013;22(12):3572–6.
Duruibe JO, Ogwuegbu MOC, Egwurugwu JN. Heavy metal pollution and human biotoxic effects. Int J Phys Sci. 2007;2(5):112–8.
Tripathi RM, Raghunath R, Krishnamoorthy TM. Dietary intake of heavy metals in Bombay city, India. Sci Total Environ. 1997;208(3):149–59.
Gerhard I, Monga B, Waldbrenner A, Runnebaum B. Heavy metals and fertility. J Toxicol Environ Health A. 1998;54:593–612.
Chowdhury AR. Recent Advances in Heavy Metals Induced Effect on Male Reproductive Function—A Retrospective. Al Ameen J Med Sci. 2009;2(2):37–42.
Shukor MY, Masdor N, Baharom NA, Jamal JA, Abdullah MP., Shamaan NA, et al. An inhibitive determination method for heavy metals using bromelain, a cysteine protease. Appl Biochem Biotechnol. 2008;144(3):283–91.
Parkinson A. Biotransformation of xenobiotics. McGraw-Hill New York; 2001.
Ahmad SA, Shamaan NA, Arif NM, Koon GB, Shukor MYA, Syed MA. Enhanced phenol degradation by immobilized Acinetobacter sp. strain AQ5NOL 1. World J Microbiol Biotechnol. 2012;28(1):347–52.
Mehrotra S, SANDHIR R, Chandra D. Degradation of Xenobiotics and Bioremediation. Environ Microbiol Biotechnol. 2004;59.
Varanasi U, Stein JE. Disposition of xenobiotic chemicals and metabolites in marine organisms. Environ Health Perspect. 1991;90:93.
Abhilash PC, Singh N. Pesticide use and application: An Indian scenario. J Hazard Mater. 2009;165(1–3):1–12.
Begum G. Assessment of biochemical markers of carbofuran toxicity and recovery response in tissues of the freshwater teleost, Clarias batrachus (Linn). Bull Environ Contam Toxicol. 2008;81(5):480–4.
Begum G. Enzymes as biomarkers of cypermethrin toxicity: Response of Clarias batrachus tissues ATPase and glycogen phosphorylase as a function of exposure and recovery at sublethal level. Toxicol Mech Methods. 2009;19(1):29–39.
Tham LG, Perumal N, Syed MA, Shamaan NA, Shukor MY. Assessment of Clarias batrachus as a source of acetylcholinesterase (AChE) for the detection of insecticides. J Environ Biol. 2009;30(1):135–8.
Begum G. Organ-specific ATPase and phosphorylase enzyme activities in a food fish exposed to a carbamate insecticide and recovery response. Fish Physiol Biochem. 2011;37(1):61–9.
Palanisami S, Prabaharan D, Uma L. Fate of few pesticide-metabolizing enzymes in the marine cyanobacterium Phormidium valderianum BDU 20041 in perspective with chlorpyrifos exposure. Pestic Biochem Physiol. 2009;94(2–3):68–72.
Sabullah MK. Acetylcholinesterase from Osteochilus hasselti for the detection of insecticides and heavy metals. Universiti Putra Malaysia; 2011.
Sabullah K, Ahmad SA, Ishak I, Sulaiman MR, Shukor MY, Syed MA, et al. An inhibitive assay for insecticides using the acetylcholinesterase from Osteochillus hasselti. Bull Environ Sci Manag. 2013;1(1):1–4.
Hayat NM, Sabullah MK, Shukor MY, Syed MA, Dahalan FA, Khalil KA, et al. The effect of pesticides on cholinesterase activity by using fish as a biomarker. Nanobio Bionano [Internet]. 2014 [cited 2015 Jan 12];1(1). Available from: http://journal.hibiscuspublisher.com/index.php/NAB/article/view/50
Sabullah MK, Sulaiman MR, Shukor MYA, Syed MA, Shamaan NA, Khalid A, et al. The assessment of cholinesterase from the liver of Puntius javanicus as detection of metal ions. Sci World J. 2014;2014.
Shukor M, Masdor N, Halmi M, Kamaruddin K, Syed M. Near-real-time biomonitoring of heavy metals using the xenoassay® system. Proc Annu Int Conf Syiah Kuala Univ-Life Sci Eng Chapter. 2013;3(1).
Botsford JL. A simple assay for toxic chemicals using a bacterial indicator. World J Microbiol Biotechnol. 1998;14(3):369–76.
Raj DS, Prabha RJ, Leena R. Analysis of bacterial degradation of azo dye congo red using HPLC. J Ind Pollut Control. 2012;28(1):57–62.
Gaspare L, Machiwa JF, Mdachi SJM, Streck G, Brack W. Polycyclic aromatic hydrocarbon (PAH) contamination of surface sediments and oysters from the inter-tidal areas of Dar es Salaam, Tanzania. Environ Pollut. 2009;157(1):24–34.
Kohler A, Schneider S. Macrophytes as bioindicators. Arch Hydrobiol Suppl. 2003;147(1–2):17–31.
Markert B, Wappelhorst O, Weckert V, Herpin U, Siewers U, Friese K, et al. The use of bioindicators for monitoring the heavy-metal status of the environment. J Radioanal Nucl Chem. 1999;240(2):425–9.
Thomulka KW, McGee DJ, Lange JH. Use of the bioluminescent bacterium Photobacterium phosphoreum to detect potentially biohazardous materials in water. Bull Environ Contam Toxicol. 1993;51(4):538–44.
Bitton G, Koopman B, Agami O. MetPADTM: a bioassay for rapid assessment of heavy metal toxicity in wastewater. Water Environ Res. 1992;834–6.
Shukor MY, Masdor N, Baharom NA, Jamal JA, Abdullah MPA, Shamaan NA, et al. An inhibitive determination method for heavy metals using bromelain, a cysteine protease. Appl Biochem Biotechnol. 2008;144(3):283–91.
Shukor MY, Baharom NA, Masdor NA, Abdullah MPA, Shamaan NA, Jamal JA, et al. The development of an inhibitive determination method for zinc using a serine protease. J Environ Biol. 2009;30(1):17–22.
Baskaran G, Masdor NA, Syed MA, Shukor MY. An inhibitive enzyme assay to detect mercury and zinc using protease from Coriandrum sativum. Sci World J [Internet]. 2013;2013. Available from: http://www.scopus.com/inward/record.url?eid=2-s2.0-84886463804&partnerID=40&md5=56fe4ef11ba50ff5275953a2612962c1
Gunasekaran B, Sulaiman MH, Halmi MIE, Amir S, Roslan MAH, Jirangon H, et al. An inhibitive determination method for heavy metals using tomato crude proteases. Asian J Plant Biol. 2013;1(1):10–4.
Wahab SMA, Gunasekaran B, Shaharuddin NA, Johari WLW, Halmi MIE, Said NAM, et al. A novel method for the determination of mercury in herbal preparation using an inhibitive assay based on the protease papain. J Environ Microbiol Toxicol. 2013;1(1):1–4.
Gunasekaran B, Kasim MHM, Salvamani S, Shukor MY. Field trials on heavy metals using alpha-chymotryopsin enzyme assay. J Environ Microbiol Toxicol. 2014;2(1):25–34.
Sahlani MZ, Halmi MIE, Masdor NA, Gunasekaran B, Wasoh H, Syed MA, et al. A rapid inhibitive assay for the determination of heavy metals using α-chymotrypsin; a serine protease. Nanobio Bionano. 2014;1(2):41–6.
Shukor MY, Anuar N, Halmi MIE, Masdor NA. Near real-time inhibitive assay for heavy metals using achromopeptidase. Indian J Biotechnol. 2014;13(3):398–403.
Bodar CWM, Van Leeuwen CJ, Voogt PA, Zandee DI. Effect of cadmium on the reproduction strategy of Daphnia magna. Aquat Toxicol. 1988;12(4):301–9.
De Coen WM, Janssen CR. The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations. J Aquat Ecosyst Stress Recovery Former J Aquat Ecosyst Health. 1997;6(1):43–55.
Diamantino TC, Guilhermino L, Almeida E, Soares AMVM. Toxicity of sodium molybdate and sodium dichromate to Daphnia magna Straus evaluated in acute, chronic, and acetylcholinesterase inhibition tests. Ecotoxicol Environ Saf. 2000;45(3):253–9.
Davies TD, Pickard J, Hall KJ. Acute molybdenum toxicity to rainbow trout and other fish. J Environ Eng Sci. 2005;4(6):481–5.
Shukor MY, Baharom NA, Masdor NA, Abdullah MPA, Shamaan NA, Jamal JA, et al. The development of an inhibitive determination method for zinc using a serine protease. J Environ Biol. 2009;30(1):17–22.
Kaira M, Halmi MIE, Shukor MY. Use of microorganisms, enzymes and plant proteases for heavy metals biomonitoring- a mini review. Asian J Plant Biol. 2013;1(1):20–4.
Sabullah MK, Ahmad SA, Sulaiman MR, Shukor MY, Syed MA, Shamaan NA. The development of an inhibitive assay for heavy metals using the acetylcholinesterase from Periophtalmodon schlosseri. J Environ Bioremediation Toxicol. 2013;1(1):20–4.
Sabullah MK, Sulaiman MR, Shukor MYA, Syed MA, Shamaan NA, Khalid A, et al. The assessment of cholinesterase from the liver of Puntius javanicus as detection of metal ions. Sci World J. 2014;2014.
Hayat NM, Shamaan NA, Shukor MY, Sabullah MK, Syed MA, Khalid A, et al. Cholinesterase-based biosensor using Lates calcarifer (Asian Seabass) brain for detection of heavy metals. J Chem Pharm Sci. 2015;8(2):376–81.
Sabullah MK, Ahmad SA, Shukor MY, Gansau AJ, Syed MA, Sulaiman MR, et al. Heavy metal biomarker: Fish behavior, cellular alteration, enzymatic reaction and proteomics approaches. Int Food Res J. 2015;22(2):435–54.
Sabullah MK, Sulaiman MR, Abd Shukor MY, Shamaan NA, Khalid A, Ahmad SA. In vitro and in vivo effects of Puntius javanicus cholinesterase by copper. Fresenius Environ Bull. 2015;24(12 B):4615–4621.
Sabullah MK, Sulaiman MR, Shukor MS, Yusof MT, Johari WLW, Shukor MY, et al. Heavy metals biomonitoring via inhibitive assay of acetylcholinesterase from Periophthalmodon schlosseri. Rendiconti Lincei. 2015;26(2):151–8.
Hayat NM, Shamaan NA, Sabullah MK, Shukor MY, Syed MA, Khalid A, et al. The use of Lates calcarifer as a biomarker for heavy metals detection. Rendiconti Lincei. 2016;Article in Press:1–10.
Attar H, Afshar S. Design of Sensible Biosensor for Rapid Detection of Biocides in Potable Water. Asian J Biotechnol. 2010;2(2):120–6.
Sowerby JM, Ottaway JH. The enzymic estimation of glutamate and glutamine. Biochem J. 1966;99(1):246–52.
Altman FP. Tetrazolium salts and formazans. Prog Histochem Cytochem. 1976;9(3):1–56.
Berridge MV, Tan AS. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2- yl)-2,5-diphenyltetrazolium bromide (MTT): Subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys. 1993;303(2):474–82.
Ahmad F, Halmi MIE, Baskaran G, Johari WLW, Shukor MY, Syed MA. Inhibitive bacterial MTT assay for river monitoring of heavy metals. Bioremediation Sci Technol Res. 2013;1(1):1–7.
Halmi MIE, Ahmad F, Hashim AK, Shamaan NA, Syed MA, Shukor MY. Effect of bacterial growth period on the sensitivity of the MTT assay for silver. J Environ Biol. 2014;35(2):353–5.
Isa HWM, Johari WLW, Syahir A, Shukor MA, Azwady AN, Shaharuddin N, et al. Development of a bacterialbased tetrazolium dye (MTT) assay for monitoring of heavy metals. Int J Agric Biol. 2014;16:1123–1128.
Elnabarawy MT, Robideau RR, Beach SA. Comparison of three rapid toxicity test procedures: Microtox,® polytox,® and activated sludge respiration inhibition. Toxic Assess. 1988;3(4):361–70.
Johnson BT. Microtox® acute toxicity test. In: Small-Scale Freshwater Toxicity Investigations: Volume 1 - Toxicity Test Methods. 2005. p. 69–105.
Girotti S, Ferri EN, Fumo MG, Maiolini E. Monitoring of environmental pollutants by bioluminescent bacteria. Anal Chim Acta. 2008;608(1):2–29.
Ronco AE. Development of a bioassay reagent using Photobacterium phosphoreum as a test for the detection of aquatic toxicants. World J Microbiol Biotechnol. 1992;8(3):316–8.
Girotti S, Bolelli L, Roda A, Gentilomi G, Musiani M. Improved detection of toxic chemicals using bioluminescent bacteria. Anal Chim Acta. 2002;471(1):113–20.
Hsieh C-Y, Tsai M-H, Ryan DK, Pancorbo OC. Toxicity of the 13 priority pollutant metals to Vibrio fisheri in the Microtox® chronic toxicity test. Sci Total Environ. 2004;320(1):37–50.
Onorati F, Mecozzi M. Effects of two diluents in the Microtox® toxicity bioassay with marine sediments. Chemosphere. 2004;54(5):679–87.
Liang XU, Sheng Z. The Application of Deltatox~î« Water Toxicity Detector in the Emergency Monitoring of Water Pollution. Pollut Control Technol. 2009;
Bulich AA. Use of luminescent bacteria for determining toxicity in aquatic environments. Aquat Toxicol. 1979;667:98–106.
Gellert G, Stommel A, Trujillano AB. Development of an optimal bacterial medium based on the growth inhibition assay with Vibrio fischeri. Chemosphere. 1999;39(3):467–76.
Ulitzur S, Lahav T, Ulitzur N. A novel and sensitive test for rapid determination of water toxicity. Environ Toxicol. 2002;17(3):291–6.
Mariscal A, Peinado MT, Carnero-Varo M, Fernández-Crehuet J. Influence of organic solvents on the sensitivity of a bioluminescence toxicity test with Vibrio harveyi. Chemosphere. 2003;50(3):349–54.
Peinado MT, Mariscal A, Carnero-Varo M, Fernández-Crehuet J. Correlation of two bioluminescence and one fluorogenic bioassay for the detection of toxic chemicals. Ecotoxicol Environ Saf. 2002;53(1):170–7.
Lee HJ, Villaume J, Cullen DC, Kim BC, Gu MB. Monitoring and classification of PAH toxicity using an immobilized bioluminescent bacteria. Biosens Bioelectron. 2003;18(5–6):571–7.
Hong Y, Chen Z, Zhang B, Zhai Q. Isolation of Photobacterium sp. LuB-1 and its application in rapid assays for chemical toxicants in water. Lett Appl Microbiol. 2010;51(3):308–12.
Ren S, Frymier PD. Toxicity of metals and organic chemicals evaluated with bioluminescence assays. Chemosphere. 2005;58(5):543–50.
Girotti S, Ferri EN, Fumo MG, Maiolini E. Monitoring of environmental pollutants by bioluminescent bacteria. Anal Chim Acta. 2008 Feb 4;608(1):2–29.
Dutka BJ, Kwan KK. Comparison of three microbial toxicity screening tests with the microtox test. Bull Environ Contam Toxicol. 1981 Jul;27–27(1):753–7.
Watanabe H, Hastings JW. Inhibition of bioluminescence in Photobacterium phosphoreum by sulfamethizole and its stimulation by thymine. Biochim Biophys Acta BBA - Bioenerg. 1990 Jun;1017(3):229–34.
Zahaba M, Halmi MIE, Ahmad SA, Shukor MY, Syed MA. Isolation and characterization of luminescent bacterium for sludge biodegradation. J Environ Biol. 2015;36(6):1255.
Choi SH, Gu MB. A portable toxicity biosensor using freeze-dried recombinant bioluminescent bacteria. Biosens Bioelectron. 2002;17(5):433–40.
Widder E a. Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science. 2010 May 7;328(5979):704–8.
Hastings JW, Greenberg EP. Quorum sensing: the explanation of a curious phenomenon reveals a common characteristic of bacteria. J Bacteriol. 1999;181(9):2667.
Hastings JW. Bioluminescence. Annu Rev Biochem. 1968;37(1):597–630.
Hastings J, Potrikusv CJ, Gupta SC, Kurfürst M, Makemson JC. Biochemistry and physiology of bioluminescent bacteria. Adv Microb Physiol. 1985;26:235–91.
Thomulka KW, McGee DJ, Lange JH. Use of the bioluminescent bacterium Photobacterium phosphoreum to detect potentially biohazardous materials in water. Bull Environ Contam Toxicol. 1993;51(4):538–44.
Engebrecht J, Nealson K, Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell. 1983;32(3):773–81.
Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol. 2005;21:319–46.
Kaiser KL., Palabrica VS. Photobacterium phosphoreum toxicity data index. Water Qual Res J Can. 1991;26(3):361–431.
Halmi MIE, Johari WLW, Amir S, Sulaiman R, Azlina A, Shukor MY, et al. Monitoring of heavy metals level in fish using Photobacterium sp. strain MIE. Bioremediation Sci Technol Res. 2013;1(1):19–22.
Abd Rachman AR, Halmi MIE, Shukor MY. Amplification of new isolated luciferase gene from marine Photobacterium strain MIE by using specific PCR. J Environ Microbiol Toxicol. 2014;2(1):35–7.
Parvez S, Venkataraman C, Mukherji S. A review on advantages of implementing luminescence inhibition test (Vibrio fischeri) for acute toxicity prediction of chemicals. Environ Int. 2006;32(2):265–8.
Salizzato M, Bertato V, Pavoni B, Ghirardini AV, Ghetti PF. Sensitivity limits and EC50 values of the Vibrio fischeri test for organic micropollutants in natural and spiked extracts from sediments. Environ Toxicol Chem. 1998;17(4):655–61.
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