Abstract
This study provides information on the effects of inorganic and organic constituents on inactivation and sub-lethal injury of Escherichia coli in water stored in a copper vessel. E. coli suspensions were stored for up to 24 h in copper vessels containing one of the following dissolved constituents at 1 g/l: salts of inorganic ions, carbohydrates, proteins and complex natural organic mixtures. Samples were surface plated onto (i) nutrient agar, incubated under standard aerobic conditions to provide conventional counts for uninjured bacteria count and onto (ii) nutrient agar plates with 0.5 g/l sodium pyruvate incubated under anaerobic conditions to enumerate sub-lethally injured (oxygen-sensitive) bacteria alongside their healthy counterparts. The concentration of dissolved copper in the stored water was determined using atomic absorption spectrophotometry. The addition of chloride salts resulted in a faster inactivation of E. coli compared to pure water with no dissolved additives, irrespective of the counterion. In contrast, a slower inactivation was observed in the presence of Na2SO4, NaNO3 and NaNO2 when compared to NaCl. Addition of the carbohydrates glucose, lactose and starch gave broadly similar results to those obtained using unsupplemented water. However, the addition of amino acids, proteins, humic acid or complex organic mixtures caused a dramatic decrease in inactivation of E. coli, with evidence of a greater number of sub-lethally injured bacteria than was seen with other added constituents. The amount of copper was highest in stored water containing amino acids and complex organic constituents, with the slow inactivation most likely to be due to complex formation between leached copper and these organic constituents. The present study clearly demonstrates that water composition, particularly natural organic constituents, has a substantial impact on the antibacterial effectiveness and dissolved copper concentration of water stored in copper vessels and that both aspects will need to be considered in terms of their impact on the practical use of copper-based systems for small-scale water treatment.
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Abbreviations
- ROS:
-
Reactive oxygen species
- CPCB:
-
Central Pollution Control Board of India
- BSA:
-
Bovine serum albumin
- AAS:
-
Atomic absorption spectrophotometry
References
Achat ST, Raju VB, Sriramachari S (1960) Indian childhood cirrhosis. Trop Pediatr 57:744–758
Aldsworth TG, Sharman RL, Dodd CER (1999) Bacterial suicide through stress. Cell Mol Life Sci 56:378–383
Alonso JL, Soriano A, Carbajo O, Amoros I, Garelick H (1999) Comparison and recovery of E. coli and thermotolerant coliforms in water with a chromogenic medium incubated at 41 and 44.5°C. Appl Environ Microbiol 65:3746–3749
Ashworth DJ, Alloway BJ (2007) Complexation of copper by sewage sludge-derived dissolved organic matter: effects on soil sorption behaviour and plant uptake. Water Air Soil Pollut 182:187–196
Belly RT, Kydd GC (1981) Silver resistance in microorganisms. Dev Ind Microbiol 23:567–578
Bhave SA, Pandit AN, Tanner MS (1987) Comparison of feeding history of children with Indian childhood cirrhosis and paired controls. J Pediatr Gastroenterol Nutr 6:562–567
Bitton G, Freihofer V (1977) Influence of extracellular polysaccharides on the toxicity of copper and cadmium towards Klebsiella aerogenes. Microb Ecol 4:119–125
Bremner I (1998) Manifestations of copper excess. Am J Clin Nutr 67:1069S–1073S
Brick T, Primrose B, Chandrasekhar R, Roy S, Muliyil J, Kang G (2004) Water contamination in urban south India: household storage practices and their implications for water safety and enteric infections. Int J Hyg Environ Health 207:473–480
Broo AE, Berghult B, Hedberg T (1997) Copper corrosion in drinking water distribution systems-the influence of water quality. Corr Sci 39:1119–1132
Bryan SE, Tipping E, Taylor-Hamilton J (2002) Comparison of measured and modelled copper binding by natural organic matter in freshwaters. Comp Biochem Physiol C 133:37–49
Buffle J (1988) Complexation reaction in aquatic system. An analytical approach. Ellis-Horwood, Chichester
Central Pollution Control Board of India (2007) Status of water quality in India. Ministry of Environment and Forests, Delhi
Chen J, Tendeyong F, Yiacoumi S (1997) Equilibrium and kinetic studies of copper ion uptake by calcium alginate. Environ Sci Technol 31:1433–1439
Danks DM (1991) Copper and the liver disease. Eur J Pediatr 150:142–148
De Spiegeleer P, Sermon J, Lietaert A, Aertsen A, Michiels CW (2004) Source of tryptone in growth medium affects oxidative stress resistance in Escherichia coli. J Appl Microbiol 97:124–133
DeNormandie J, Sunita J (2002) Combating diarrhoeal disease in India through safe drinking water. World Health Organisation (WHO). http://www.who.int/mediacentre/multimedia/2002/ind_sanitation/en/index.htmL
Deschamps P, Zerrouk N, Nicolis I, Martens T, Curis E, Charlot MF, Girerd JJ, Prange T, Benazeth S, Chaumeil JC, Thomas A (2003) Copper(II)-/L-glutamine complexation study in solid state and in aqueous solution. Inorg Chim Acta 353:22–34
Duthil JP, Mankowski G, Giusti A (1996) The synergetic effect of chloride and sulphate on pitting corrosion of copper. Corr Sci 38:1839–1849
Eife R, Weiss M, Barros V, Sigmund B, Goriup U, Komb D, Wolf W, Kittel J, Schramel P, Reiter K (1999) Chronic poisoning by copper in tap water: I. Copper intoxications with predominantly gastrointestinal symptoms. Eur J Med Res 28:219–223
Fukushi K, Chang D, Ghosh S (1996) Enhanced heavy metal uptake by activated sludge cultures grown in the presence of biopolymer stimulators. Water Sci Technol 34:272–276
Fukushi K, Kato S, Antsuki T, Omura T (2001) Isolation of copper-binding proteins from activated sludge culture. Water Sci Technol 44:453–459
Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicol 189:147–163
Ge X, Wang X, Seetharaman S (2009) Copper extraction from copper ore by electro-reduction in molten CaCl2–NaCl. Electrochim Acta 54:4397–4402
Ghosh S, Bupp S (1992) Stimulation of biological uptake of heavy metals. Water Sci Technol 26:227–236
Hamilton WP, Kim M, Thackston EL (2005) Comparison of commercially available Escherichia coli enumeration tests: implications for attaining water quality standards. Water Res 39:4869–4878
Herreros O, Vinals J (2007) Leaching of sulfide and copper ore in a H2SO4–O2 media with acid pre-treatment. Hydrometallurgy 89:260–268
Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD (2002) Manual of environmental microbiology, 2nd edn. ASM Press, Washington, DC
Karlsson T, Persson P, Skyllberg U (2006) Complexation of copper (II) in organic soils and in dissolved organic matter–EXAFS evidence for chelate ring structures. Environ Sci Technol 40:2623–2628
Kear G, Barker BD, Walsh FC (2004) Electrochemical corrosion of unalloyed copper in chloride media-—critical review. Corr Sci 46:109–135
Khaengraeng R, Reed RH (2005) Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol 99:39–50
Klotz LO, Kroencke KD, Buchczyk DP, Sies H (2003) Role of copper, zinc, selenium, and telluriumin the cellular defense against oxidative and nitrosative stress. J Nutr 133:448S–1451S
Kosek M, Bern C, Guerrant RL (2003) The magnitude of the global burden of diarrhoeal disease from studies published 1992–2000. Bull World Health Organ 81:197–204
Kosec T, Milosev I, Pihlar B (2007) Benzotriazole as an inhibitor of brass corrosion in chloride solution. Appl Surf Sci 253:8863–8873
Leclerc H, Mossel DAA, Edberg SC, Struijk CB (2001) Advances in the bacteriology of the coliform group: their suitability as markers of microbial water safety. Annu Rev Microbiol 55:201–234
Linder MC (1990) The biochemistry of copper. Plenum Press, New York
Lindskog RU, Lindskog PA (1988) Bacteriological contamination of water in rural areas: an intervention study from Malawi. J Trop Med Hyg 91:1–7
Maggini S, Wintergerst ES, Beveridge S, Hornig DH (2007) Selected vitamins and trace elements support immune function by strengthening epithelial barriers and cellular and humoral immune responses. Brit J Nutr 98:S29–S35
Mamas S, Kiyak T, Kabasakaloglu M, Koc A (2005) The effect of benzotriazole on brass corrosion. Mater Chem Phys 93:41–47
Masuoka J, Saltman P (1994) Zinc(II) and copper(II) binding to serum albumin. A comparative study of dog, bovine, and human albumin. J Biol Chem 269:25557–25561
Micheletti E, Pereira S, Mannelli F, Ferreira PM, Tamagnini P, Philippis R (2008) Sheathless mutant of the cyanobacterium Gloeothece sp. strain PCC 6909 with increased capacity to remove copper ions from aqueous solutions. Appl Environ Microbiol 74:2797–2804
Müller-Höcker, Meyer U, Wiebecke B et al (1988) Copper storage disease of the liver and chronic dietary copper intoxication in two further German infants mimicking Indian childhood cirrhosis. Pathol Res Pract 183:39–45
Natale GD, Damante CA, Nagy Z, Osz K, Pappalardo G, Rizzarelli E, Sovago I (2008) Copper(II) binding to two novel histidine-containing model hexapeptides: Evidence for a metal ion driven turn conformation. J Inorgan Biochem 102:2012–2019
Olivares M, Uauy R (1996) Copper as an essential nutrient. Am J Clin Nutr 791S–96S
Pan YJ, Loo G (2000) Effect of copper deficiency on oxidative DNA damage in Jurkat T-lymphocytes. Free Rad Biol Med 28:824–830
Percival SS (1988) Copper and immunity. Am J Clin Nutr 67:1064S–1085S
Reed RH (2004) The inactivation of microbes by sunlight: solar disinfection as a water treatment process. Adv Appl Microbiol 54:333–365
Roberts L, Chartier Y, Chartier O, Malenga G, Toole M, Rodka H (2001) Keeping clean water clean in a Malawi refugee camp: a randomized intervention trial. Bull World Health Organ 79:280–287
Sharan R, Chhibber S, Attri S, Reed RH (2010) Inactivation and injury of Escherichia coli in a copper water storage vessel: effects of temperature and pH. Ant van Leeuwen 97:91–97
Sokic MD, Markovic B, Zivkovic D (2009) Kinetics of chalcopyrite leaching by sodium nitrate in sulphuric acid. Hydrometallurgy 95:273–279
Sovago I, Osz K (2006) Metal ion selectivity of oligopeptides. Dalton Trans 3841–3854
Stephens PJ, Druggan P, Caron NV (2000) Stressed Salmonella are exposed to reactive oxygen species from two independent sources during recovery in conventional culture media. Int J Food Microbiol 60:269–285
Sudha VBP, Singh KO, Prasad SR, Venkatasubramanian P (2009) Killing of enteric bacteria in drinking water by a copper device for use in home: laboratory evidence. Trans Roy Soc Trop Med Hyg 103:819–822
Tambe PV, Daswani PG, Mistry NF, Ghadge AA, Antia NH (2008) A community-based bacteriological study of quality of drinking water and its feedback to a rural community in western Maharashtra, India. J Health Popul Nutr 26:139–150
Tandon P, Chhibber S, Reed RH (2005) Inactivation of Escherichia coli and coliform bacteria in traditional brass earthernware water storage vessels. Ant van Leeuw 88:35–48
Tipping E (2002) Cation binding by humic substances. Cambridge Environmental Chemistry series, vol 12. Cambridge University Press, Cambridge
Trevett AF, Carter RC (2008) Targeting appropriate interventions to minimize deterioration of drinking water quality in developing countries. J Health Popul Nutr 26:125–138
Vanderslice J, Briscoe J (1993) All coliforms are not created equal—a comparison of the effects of water source and in-house water contamination on infantile diarrheal disease. Water Resources Res 29:1983–1995
Villamil RFV, Corio P, Rubim JC, Agostinho SML (2002) Sodium dodecylsulfate–benzotriazole synergistic effect as an inhibitor of processes on copper chloridric acid interfaces. J Electroanal Chem 535:75–83
Wright J, Gundry S, Conroy R (2004) Household drinking water in developing countries: a systematic review of microbiological contamination between source and point-of-use. Trop Med Int Health 9:106–117
Zhang LM, Chen DQ (2002) An investigation of adsorption of lead(II) and copper(II) ions by water-insoluble starch graft copolymers. Colloids Surf A Physicochem Eng Aspects 205:231–236
Acknowledgement
The authors wish to thank the US Copper Development Association and Harold Michels for providing the funding support for the study.
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Sharan, R., Chhibber, S., Attri, S. et al. Inactivation and sub-lethal injury of Escherichia coli in a copper water storage vessel: effect of inorganic and organic constituents. Antonie van Leeuwenhoek 98, 103–115 (2010). https://doi.org/10.1007/s10482-010-9435-3
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DOI: https://doi.org/10.1007/s10482-010-9435-3