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Inactivation and sub-lethal injury of Escherichia coli in a copper water storage vessel: effect of inorganic and organic constituents

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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

    Google Scholar 

  • Aldsworth TG, Sharman RL, Dodd CER (1999) Bacterial suicide through stress. Cell Mol Life Sci 56:378–383

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Belly RT, Kydd GC (1981) Silver resistance in microorganisms. Dev Ind Microbiol 23:567–578

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bitton G, Freihofer V (1977) Influence of extracellular polysaccharides on the toxicity of copper and cadmium towards Klebsiella aerogenes. Microb Ecol 4:119–125

    Article  Google Scholar 

  • Bremner I (1998) Manifestations of copper excess. Am J Clin Nutr 67:1069S–1073S

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Broo AE, Berghult B, Hedberg T (1997) Copper corrosion in drinking water distribution systems-the influence of water quality. Corr Sci 39:1119–1132

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Buffle J (1988) Complexation reaction in aquatic system. An analytical approach. Ellis-Horwood, Chichester

    Google Scholar 

  • Central Pollution Control Board of India (2007) Status of water quality in India. Ministry of Environment and Forests, Delhi

    Google Scholar 

  • Chen J, Tendeyong F, Yiacoumi S (1997) Equilibrium and kinetic studies of copper ion uptake by calcium alginate. Environ Sci Technol 31:1433–1439

    Article  CAS  Google Scholar 

  • Danks DM (1991) Copper and the liver disease. Eur J Pediatr 150:142–148

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Duthil JP, Mankowski G, Giusti A (1996) The synergetic effect of chloride and sulphate on pitting corrosion of copper. Corr Sci 38:1839–1849

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Fukushi K, Kato S, Antsuki T, Omura T (2001) Isolation of copper-binding proteins from activated sludge culture. Water Sci Technol 44:453–459

    CAS  PubMed  Google Scholar 

  • Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicol 189:147–163

    Article  CAS  Google Scholar 

  • Ge X, Wang X, Seetharaman S (2009) Copper extraction from copper ore by electro-reduction in molten CaCl2–NaCl. Electrochim Acta 54:4397–4402

    Article  CAS  Google Scholar 

  • Ghosh S, Bupp S (1992) Stimulation of biological uptake of heavy metals. Water Sci Technol 26:227–236

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Herreros O, Vinals J (2007) Leaching of sulfide and copper ore in a H2SO4–O2 media with acid pre-treatment. Hydrometallurgy 89:260–268

    Article  CAS  Google Scholar 

  • Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD (2002) Manual of environmental microbiology, 2nd edn. ASM Press, Washington, DC

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kear G, Barker BD, Walsh FC (2004) Electrochemical corrosion of unalloyed copper in chloride media-—critical review. Corr Sci 46:109–135

    Article  CAS  Google Scholar 

  • Khaengraeng R, Reed RH (2005) Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol 99:39–50

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Kosec T, Milosev I, Pihlar B (2007) Benzotriazole as an inhibitor of brass corrosion in chloride solution. Appl Surf Sci 253:8863–8873

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Linder MC (1990) The biochemistry of copper. Plenum Press, New York

    Google Scholar 

  • Lindskog RU, Lindskog PA (1988) Bacteriological contamination of water in rural areas: an intervention study from Malawi. J Trop Med Hyg 91:1–7

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mamas S, Kiyak T, Kabasakaloglu M, Koc A (2005) The effect of benzotriazole on brass corrosion. Mater Chem Phys 93:41–47

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Percival SS (1988) Copper and immunity. Am J Clin Nutr 67:1064S–1085S

    Google Scholar 

  • Reed RH (2004) The inactivation of microbes by sunlight: solar disinfection as a water treatment process. Adv Appl Microbiol 54:333–365

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sokic MD, Markovic B, Zivkovic D (2009) Kinetics of chalcopyrite leaching by sodium nitrate in sulphuric acid. Hydrometallurgy 95:273–279

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tipping E (2002) Cation binding by humic substances. Cambridge Environmental Chemistry series, vol 12. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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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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Correspondence to Robert H. Reed.

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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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