Effect of Copper Chemical Form on The Growth of Pseudomonas aeruginosa Isolated from Burned Patients and on Its Cu Uptake

Main Article Content

Amjad Al Tarawneh
Haitham Qaralleh
Muhamad Al-limoun
Khaled Khleifat


The main object of this investigation was to shed light on the information on the level of Cu uptake by Pseudomonas aeruginosa that has been previously isolated from patients using Gram-negative E. aerogenes ans a Gram-positive Bacillus thuringiensis as a control for Cu uptake measurements. Cu uptake data showed that maximum Cu uptake was obtained by the Pseudomonas aeruginosa. The metal uptake was dependent on the type of biosorbent with different accumulation affinities toward the tested chemical form of the copper. Cells harvested at exponential growth phase showed slightly higher Cu uptake than at stationary phase, which reflect that the Cu uptake is metabolism dependent-process. The increasing order of affinity of the cupric chloride and cupric sulphate towards the three genera were almost constant. However, where cupric nitrate was used, the copper uptake behavior in Pseudomonas aeroginosa was not changed from those results with the other two chemical forms, whereas with E.  aerogenes & B. thuringiensis, different Cu uptake behaviors were observed. In B. thuengenesis, the copper uptake rate as a function of initial Cu concentration were shown to increase with increasing the initial concentration of Cu, constantly above 320 ppm as compared with others. In Enterobacter with cupric nitrate, different bahavior was also shown in which the copper uptake decline sharply beyond the 320 ppm. These results reflect that the Cu uptake in P. aeruginosa is with different mechanisms as compared with other tested bacteria


Download data is not yet available.


Metrics Loading ...

Article Details



Abboud, M. M., Saeed, H. A., Tarawneh, K. A., Khleifat, K. M., & Al Tarawneh, A. (2009). Copper uptake by Pseudomonas aeruginosa isolated from infected burn patients. Current microbiology, 59(3), 282-287.

Abboud, M. M., Aljundi, I. H., Khleifat, K. M., & Dmour, S. (2010). Biodegradation kinetics and modeling of whey lactose by bacterial hemoglobin VHb-expressing Escherichia coli strain. Biochemical Engineering Journal, 48(2), 166-172.

Althunibat, O. Y., Qaralleh, H., Al-Dalin, S. Y. A., Abboud, M., Khleifat, K., Majali, I. S., ... & Jaafraa, A. (2016). Effect of thymol and carvacrol, the major components of Thymus capitatus on the growth of Pseudomonas aeruginosa. J Pure Appl Microbiol, 10, 367-74.

Bodey G P, Bolivar R, Fainstain V, Jadeja L ( 1983). Infections caused by Pseudomonas aeruginosa. Rev. Infect. Dis. 5: 279-313.

Botzenhart K, Doring G (1993). Ecology and epidemiology of Pseudomonas aeruginosa. New York: Plenum Press, pp. 1-18.

Chen X , Shi J, Chen Y , Xu X , Xu S , Wang Y (2006). Copper removal from aqueous systems: Biosorption by Pseudomonas syringae .Canad. J. Microbiol. 52: 308-316.

Chen Y S, Liu Y C, Yen M Y , Wang J H , Wang J H , Wann S R , Cheng D L (1997).Skin and soft-tissue manifestations of Shewanella putrefaciens infection. Clin Infect Dis.25 : 225-9.

Chan S, Garson B, Subramanian S(1998).The role of copper, molybdenum, selenium, and zinc in nutrition and health. Clin Lab Med. 18: 673-685.

Cooksey D A (1994). Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol. Rev.14: 381-386.

Cox C D (1989). Importance of iron in bacterial virulence. Metal ions and bacteria. John Wiley & Sons, Inc., New York, pp.207-246.

Dance D A B , Wuthiekanun V, Naigowit P ,White N J (1989). Identification of Pseudomonas pseudomallei in clinical practice: Use of simple screening tests and API 20 NE. J. Clin. Pathol. 42: 645-648.

Hall C , Wales D S, Keane M A ( 2001). Copper removal from aqueous systems: Biosorption by Pseudomonas syringae. Separation Science and Technology. 36: 223-240.

Hussein H , Farag S , Kandil K , Moawad H (2005). Tolerance and uptake of heavy metals by Pseudomonads .Process Biochemistry 40: 955-961

Khase S, Jande J M (1998). Biochemical and chemical properties of Shewanella alga and Shewanella putrefaciens. J Clinical Microbiology. 36 : 783-787.

Khleifat, K. M., Al-limoun, M. O., Alsharafa, K. Y., Qaralleh, H., & Al Tarawneh, A. A. (2019). Tendency of using different aromatic compounds as substrates by 2, 4-DNT dioxygenase expressed by pJS39 carrying the gene dntA from Burkholderia sp. strain DNT. Bioremediation Journal, 23(1), 22-31.

Khleifat, K. M. (2010). Characterization of 2, 4-Dinitrotoluene Dioxygenase from Recombinant Esherichia coli Strain PFJS39: Its Direct Interaction with Vitreoscilla Hemoglobin. Bioremediation Journal, 14(1), 38-53.

Khleifat, K. M., Hanafy, A. M. M., & Al Omari, J. (2014). Prevalence and molecular diversity of Legionella pneumophila in domestic hot water systems of private apartments. British Microbiology Research Journal, 4(3), 306.

Khleifat, K. M., Sharaf, E. F., & Al-limoun, M. O. (2015). Biodegradation of 2-chlorobenzoic acid by Enterobacter cloacae: Growth kinetics and effect of growth conditions. Bioremediation Journal, 19(3), 207-217.

Khleifat, K. M. (2007). Effect of substrate adaptation, carbon starvation and cell density on the biodegradation of phenol by Actinobacillus sp. Fresenius Environmental Bulletin, 16(7), 726-730.).

Khleifat, K., & Abboud, M. M. (2003). Correlation between bacterial haemoglobin gene (vgb) and aeration: their effect on the growth and ??amylase activity in transformed Enterobacter aerogenes. Journal of applied microbiology, 94(6), 1052-1058.

Khleifat, K. M. (2006). Correlation Between Bacterial Hemoglobin and Carbon Sources: Their Effect on Copper Uptake by Transformed E. coli Strain ?DH5. Current microbiology, 52(1), 64-68.

Khleifat, K. M., Abboud, M. M., & Al-Mustafa, A. H. (2006a). Effect of Vitreoscilla hemoglobin gene (vgb) and metabolic inhibitors on cadmium uptake by the heterologous host Enterobacter aerogenes. Process Biochemistry, 41(4), 930-934.

Khleifat, K. M., Tarawneh, K. A., Wedyan, M. A., Al-Tarawneh, A. A., & Al Sharafa, K. (2008). Growth kinetics and toxicity of Enterobacter cloacae grown on linear alkylbenzene sulfonate as sole carbon source. Current microbiology, 57(4), 364-370.

Khleifat, K. M., Abboud, M., Laymun, M., Al-Sharafa, K., & Tarawneh, K. (2006b). Effect of variation in copper sources and growth conditions on the copper uptake by bacterial hemoglobin gene (vgb) bearing E. coli. Pakistan Journal of Biological Sciences, 9(11), 2022-2031.

Khleifat, K., & Homady, H. M. (2000). Bacterial hemoglobin gene (vgb) transformed into Escherichia coli enhances lead-uptake and minimizes it’s adsorption. Pakistan Journal of Biological Sciences, 3(9), 1480-1483.

Klevay, L. M. (2000). Cardiovascular disease from copper deficiency—a history. The Journal of nutrition, 130(2), 489S-492S.

Linder, M. C., & Hazegh-Azam, M. (1996). Copper biochemistry and molecular biology. The American journal of clinical nutrition, 63(5), 797S-811S.

Linder, M. C., Lomeli, N. A., Donley, S., Mehrbod, F., Cerveza, P., Cotton, S., & Wooten, L. (1999). Copper transport in mammals. In Copper Transport and Its Disorders (pp. 1-16). Springer, Boston, MA.

Lu Z H, Solioz M (2001).Copper-induced proteolysis of the Cop Z copper chaperone of Enterococcus hirae. J.Biol.Chem.276 : 47822-47827.

Majali, I. S., Oran, S. A., Khaled, M. K., Qaralleh, H., Rayyan, W. A., & Althunibat, O. Y. (2015). Assessment of the antibacterial effects of Moringa peregrina extracts. African Journal of microbiology research, 9(51), 2410-2414.

McManus, A. T., Mason, A. D., McManus, W. F., & Pruitt, B. A. (1985). Twenty-five year review ofPseudomonas aeruginosa bacteremia in a burn center. European journal of clinical microbiology, 4(2), 219-223.

Nikadio H (1994). Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science. 264: 382-388.

Nikadio H (1996). Multidrug efflux pumps of Gram-negative bacteria. J. Bacteriol. 178 : 5853-5859.

Ochsner A , Johnson Z ,Vasil M L (2000). Genetics and regulation of two distinct haem-uptake systems in Pseudomonas aeruginosa. Microbiology.146: 185-198.

Olivares M ,Uauy R (1996).Copper as an essential nutrient. Am J Clin Nutr 63: 791S - 796S.

Pena M M O , Lee J, Thiele D J (1999).A delicate balance: homeostatic control of copper up take and distribution. J. Nutr. 129: 1251-1260.

Pagani, L, Lang A , Vedovelli C , Moling O, Rimenti G , Pristerà R , Mian P (2003). Soft tissue infection and bacteraemia caused by Shewanella putrefaciens. J Clinical Microbiology.41: 2240-2241.

Rasoloson, D., Shi, L., Chong, C. R., Kafsack, B. F., & Sullivan Jr, D. J. (2004). Copper pathways in Plasmodium falciparum infected erythrocytes indicate an efflux role for the copper P-ATPase. Biochemical Journal, 381(3), 803-811.

Reid D W , Withers L , Francis N J ,Wilson J W , Kotsimbos T C ( 2002). Iron deficiency in cystic fibrosis: relationship to lung disease severity and chronic Pseudomonas aeruginosa infection. Chest .121: 48-54.

Silver, S. (1996). Bacterial resistances to toxic metal ions-a review. Gene, 179(1), 9-19.

Shankowsky, H. A., Callioux, L. S., & Tredget, E. E. (1994). North American survey of hydrotherapy in modern burn care. The Journal of burn care & rehabilitation, 15(2), 143-146.

Tarawneh, K. A., Halasah, Z. A., Khleifat, A. M., Batarseh, M. I., Khleifat, K. M., & Al-Mustafa, A. H. (2011). Evaluation of cefaclor oral suspensions stability using reversed phase high performance liquid chromatography and antimicrobial diffusion methods. Pakistan journal of pharmaceutical sciences, 24(3).

Teitzel, G. M., Geddie, A., Susan, K., Kirisits, M. J., Whiteley, M., & Parsek, M. R. (2006). Survival and growth in the presence of elevated copper: transcriptional profiling of copper-stressed Pseudomonas aeruginosa. Journal of bacteriology, 188(20), 7242-7256.

Vivas, A., Biro, B., Ruiz-Lozano, J. M., Barea, J. M., & Azcon, R. (2006). Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere, 62(9), 1523-1533.

Wang, C. L., Michels, P. C., Dawson, S. C., Kitisakkul, S., Baross, J. A., Keasling, J. D., & Clark, D. S. (1997). Cadmium removal by a new strain of Pseudomonas aeruginosa in aerobic culture. Appl. Environ. Microbiol., 63(10), 4075-4078.

Yoneyama H, Nakae T (1996).Protein C (OprC) of the outer membrane of Pseudomonas aeruginosa is a copper-regulated channel protein. Microbiology. 142 :2137-44.

Yang C H, Menge J A ,Cooksey D A (1993). Role of copper resistance in competitive survival of Pseudomonas fluorescens in soil. Appl Environ Microbiol. 59: 580-584

Most read articles by the same author(s)