Sources and mechanisms of combined heavy-metal and antibiotic resistance traits in bacteria

Authors

  • Claudia ȚUGUI Department of Molecular Biology and Biotechnology, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania.
  • Edina SZEKERES Department of Molecular Biology and Biotechnology, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania; National Institute of Research and Development for Biological Sciences (NIRDBS), Institute of Biological Research, Cluj-Napoca, Romania. https://orcid.org/0000-0003-1463-6301
  • Andreea BARICZ National Institute of Research and Development for Biological Sciences (NIRDBS), Institute of Biological Research, Cluj-Napoca, Romania. *Corresponding author: andreea.baricz@icbcluj.ro https://orcid.org/0000-0003-1307-3172

DOI:

https://doi.org/10.24193/subbb.2017.1.07

Keywords:

agriculture, antibiotic resistance, aquaculture, heavy metal resistance.

Abstract

Nowadays, antibiotic resistance poses a great threat to the health of the individuals worldwide. In this context, scientific interest on how bacteria adapt in stress-related environmental conditions like those enriched in heavy metals and how the heavy-metal adaptive mechanism influence the antibiotic resistance is increasing. It was noted that the simultaneous use of heavy metals and antibiotics in agriculture and aquaculture might positively impact the dissemination of the antibiotic resistance genes in the environment. Current knowledge on the sources of simultaneous pollution with heavy metals and antibiotics, the co-occurrence of heavy-metal and antibiotic resistance traits in bacteria altogether with physiological mechanism underlying this phenomenon are overviewed.

Tugui et al (PDF)

References

Altug, G., Balkis, N. (2009) Levels of some toxic elements and frequency of bacterial heavy metal resistance in sediment and sea water, Environ. Monit. Assess., 149:61–69

Amachawadi, R. G., Scott, H. M., Alvarado, C. A., Mainini, T.R., Vinasco, J., Drouillard, J. S., Nagarajaa, T. G. (2013) Occurrence of the transferable copper resistance gene tcrb among fecal Enterococci of U.S. feedlot cattle fed copper-supplemented diets, Appl. Environ. Microbiol., 79:4369–4375

Amador, P. P., Fernandes, R. M., Prudêncio, M. C., Barreto, M. P., Duarte, I. M. (2015) Antibiotic resistance in wastewater: occurrence and fate of Enterobacteriaceae producers of class A and class C β-lactamases, J. Environ. Sci. Health A Tox. Hazard Subst. Environ. Eng., 50:26-39

Baker-Austin, C., Wright, M. S., Stepanauskas, R., McArthura, J. V. (2006) Co-selection of antibiotic and metal resistance, Trends Microbiol., 14:176-182

Banu, C., Preda, N. Vasu, S. (1982) Produsele alimentare și inocuitatea lor, Ed. Tehnică, București, pp. 404-420 [In Romanian]

Berg, J., Tom-Petersen, A., Nybroe, O. (2005) Copper amendment to agricultural soil selects for bacterial antibiotic resistance in the field, Lett. Appl. Microbiol., 40:146–151

Binggan, W., Linsheng, Y. (2010) A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China, Microchem. J., 94(2):99-107

Budambula, N. M. L., Kinyua, D. M. (2013) Antibiotic resistance of metal tolerant bacteria isolated from soil in Juja, Kenya, Conference Paper: JKUAT Scientific, Technological and Industrialization Conference November 2013, Nairobi

Chen, S., Li, X., Sun, G., Zhang, Y., Su, J., Ye, J. (2015) Heavy metal induced antibiotic resistance in bacterium LSJC7, Int. J. Mol. Sci., 16:23390-23404

Costa, R. A., Araújo, R. L., Souza, O. V., Silva dos Fernandes, R. H., Vieira, R. H. (2015) Antibiotic-Resistant Vibrios in Farmed Shrimp, Biomed. Res. Int., 1-5

D’Costa ,V. M., King, C. E., Kalan, L., Morar, M., Sung, W. W. L., Schwarz, C., Froese, D., Zazula, G., Calmels, F., Debruyne, R., Golding, G. B., Poinar, H. N., Wright, G. D. (2011) Antibiotic resistance is ancient, Nature, 477:457-461

delCastillo, I., Vizán, J. L., Rodríguez-Sáinz, M. C., Moreno, F. (1991) An unusual mechanism for resistance to the antibiotic coumermycin A1, Proc. Natl. Acad. Sci U. S. A., 88(19):8860-8864

Devika, L., Rajaram, R., Mathivanan, K. (2013) Multiple Heavy Metal and Antibiotic Tolerance Bacteria Isolated from Equatorial Indian Ocean, Int. J. Microbiol. Res., 4: 212-218

Fair, R. J., Tor, Y. (2014) Antibiotics and Bacterial Resistance in the 21st Century, Perspect. Medicin. Chem., 6:25–64

Forrest, H. N. (2012) History of zinc in agriculture, Adv. Nutr. 3:783–789

Forsberg, K. J., Reyes A., Wang, B., Selleck, E. M., Sommer, M. O. A., Dantas, G. (2012) The shared antibiotic resistome of soil bacteria and human pathogens, Science, 337: 1107–1111

Gao, X., Chen, C. T. A. (2012). Heavy metal pollution status in surface sediments of the coastal Bohai Bay, Water Res., 46:1901-1911

Gerdes, K., Rasmussen, P. B., Molin, S. (1986) Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells, Proc. Natl. Acad. Sci. U. S A., 83(10):3116–3120

Gillan, D. C., Danis, B., Pernet, P., Joly, G., Dubois, P. (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment, Appl. Environ. Microbiol., 71:679–690

Guidos, R. J. (2011). Combating Antimicrobial Resistance: Policy Recommendations to Save Lives. Clin. Infect. Dis., 52:397–428

Hayashi, S., Abe, M., Kimoto, M., Furukawa, S., Nakazawa, T. (2000) The DsbA-DsbB Disulfide Bond Formation System of Burkholderia cepacia Is Involved in the Production of Protease and Alkaline Phosphatase, Motility, Metal Resistance, and Multi-Drug Resistance, Microbiol. Immunol., 44(1):41-50

Heuer, O. E, Kruse, H., Grave, K., Collignon, P., Karunasagar, I., Angulo, F. J. (2009) Human health consequences of use of antimicrobial agents in aquaculture, Clin. Infect. Dis., 49:1248–1253

Hill, D. A., Peo, E. R., Lewis, A. J., Crenshaw, J. D. (1986) Zinc-amino acid complexes for swine, J. Anim. Sci., 63:121–30

Hossain, M. M. M., Islam, M. M. (2006) Ship breaking activities and its impact on the coastal zone of Chittagong, Bangladesh: Towards sustainable management, Young Power in Social Action (YPSA), Chittagong, Bangladesh, 12-16

Hui, L., Yi-Feng, L., Williams, B. J., Blackwell, T. S., Can-Mao, X. (2011) Structure and function of OprD protein in Pseudomonas aeruginosa: From antibiotic resistance to novel therapies, Int. J. Med. Microbiol., 302(2):10

Jackson, B. P., Bertsch, P. M., Cabrera, M. L., Camberato, J. J., Seaman, J. C., Wood, C. W. (2003) Trace element speciation in poultry litter, J. Environ. Qual., 32:535–540

Jassim, S. A. A., Limoges, R. G. (2014) Natural solution to antibiotic resistance: bacteriophages ‘The Living Drugs’, World J. Microbiol. Biotechnol., 30(8):2153–2170

Jie, S., Li, M., Gan, M., Zhu, J., Yin, H., Liu, X. (2016) Microbial functional genes enriched in the Xiangjiang River sediments with heavy metal contamination, BMC Microbiol., 16:179

Jones, H. C., Tuckman, M., Murphy, E., Bradford, P. A. (2006) Identification and Sequence of a tet(M) Tetracycline Resistance Determinant Homologue in Clinical Isolates of Escherichia coli, J. Bacteriol., 188(20):7151–7164

Kacar, A., Kocyigit, A. (2013) Characterization of heavy metal and antibiotic resistant bacteria isolated from Aliaga Ship Dismantling Zone, Eastern Aegean Sea, Turkey, Int. J. Environ. Res., 7:895-902

Karimi, A., Sadeghi, G., Vaziry, A. (2011) The effect of copper in excess of the requirement during the starter period on subsequent performance of broiler chicks, J. Appl. Poult. Res., 20:203-209

Knapp, C. W., McCluskey, S. M., Singh, B. K., Colin, D. C., Hudson, G., Graham, W. D. (2011) Antibiotic Resistance Gene Abundances Correlate with Metal and Geochemical Conditions in Archived Scottish Soils, PLoS Onev., 6(11):1-6

Kohanski, M. A., Dwyer, D. J., Collins, J. J. (2010) How antibiotics kill bacteria: from targets to networks, Nature Revs. Microbiol., 8:423–435

Landers, T. F., Cohen, B., Wittum, T. E., Larson, E. L. (2012) A Review of Antibiotic Use in Food Animals: Perspective, Policy, and Potential, Public Health Rep., 127(1), 4–22

Levy, S. B. (2002) Active efflux, a common mechanism for biocide and antibiotic resistance, J. Appl. Microbiol., 92:65–71

Li, Y. X., Chen, T. B. (2005) Concentrations of additive arsenic in Beijing pig feeds and the residues in pig manure, Res. Conserv. Recy., 45:356–367

Matyar, F., Akkan, T., Uçak, Y., Eraslan, B. (2010) Aeromonas and Pseudomonas: antibiotic and heavy metal resistance species from Iskenderun Bay, Turkey (northeast Mediterranean Sea), Environ. Monit. Assess., 167:309–320

Matyar, F., Kaya, A., Dinçer, S. (2008) Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey, Sci. Total Environ., 407:279-285

Mehi, O., Bogos, B., Csörgő, B., Pál, F., Nyerges, A., Papp, B., Pál, C. (2014) Perturbation of Iron Homeostasis Promotes the Evolution of Antibiotic Resistance, Mol. Biol. Evol., 31(10):2793–2804

Morillo, J., Usero, J., Gracia, I. (2004) Heavy metal distribution in marine sediments from the southwest coast of Spain. Chemosphere, 55:431-442

Munita, J. M. Arias, C. A. (2016) Mechanisms of Antibiotic Resistance, Microbiol Spectr., 4(2):10

Nies, D.H. (2003) Efflux-mediated heavy metal resistance in prokaryotes, FEMS Microbiol. Rev., 27:313-319

Pal, C., Bengtsson-Palme, J., Kristiansson, E., Larsson, D. J. (2015) Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential, BMC Genomics, 16:964

Plum, M. L., Rink, L., Hajo, H. (2010) The Essential Toxin: Impact of Zinc on Human Health, Int. J. Environ. Res. Public Health, 7(4):1342–1365

Quero, G. M., Cassin, D., Botter, M., Perini, L., Luna, G. M. (2015) Patterns of benthic bacterial diversity in coastal areas contaminated by heavy metals, polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs), Front. Microbiol., 6: 1053

Resende, J. A., Silva, V. L., Fontes, C. O., Souza-Filho, J. A., de Oliveira, T. L. R., Coelho, C. M., César, D. E., Diniz, C. G. (2012) Multidrug-resistance and toxic metal tolerance of medically important bacteria isolated from an aquaculture system, Microbes. Environ., 27:449–455

Ruiz, N. (2003) The role of Serratia marcescens porins in antibiotic resistance, Microb. Drug Resist., 9:257–264

Sabry, S. A., Ghozlan, H. A., Abou-Zeid, D. M. (1997) Metal tolerance and antibiotic resistance patterns of a bacterial population isolated from sea water, J. Appl. Microbiol., 82:245-252

Salami, I. R., Rahmawati, S., Sutarto, R. I., Jaya, P. M. (2008) Accumulation of heavy metals in freshwater fish in cage aquaculture at Cirata Reservoir, West Java, Indonesia, Ann. N. Y. Acad. Sci., 1140:290-6

Sapkota, A., Sapkota, A. R., Kucharski, M., Burke, J., McKenzie, S., Walker, P., Lawrence, R. (2008) Aquaculture practices and potential human health risks: current knowledge and future prioritie, Environ. Int., 34:1215-1226

Sarmah, A. K., Meyer, M. T., Boxall, A. B. (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment, Chemosphere, 65(5):725-59

Seiler, C., Berendonk, T. U. (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Role and prevalence of antibiosis and the related resistance genes in the environment, Front. Microbiol., 3: 399

Silver, S. (1996) Bacterial heavymetal resistance: new surprises, Ann. Rev. Microb., 50: 753–789

Stepanauskas, R., Glenn, T. C., Jagoe, C. H., Tuckfield, R. C., Lindell, A. H., King, C. J., McArthur, J. V. (2006) Coselection for microbial resistance to metals and antibiotics in freshwater microcosms, Environ Microbiol., 8(9):1510-1514

Szekeres, E., Baricz, A., Chiriac, C. M., Farkaș, A., Opris, O., Soran, M. L., Andrei, A. S., Rudi, K., Balcázar, J. L., Dragos, N., Coman, C. (2017) Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals, Environ. Poll., http://doi.org/10.1016/j.envpol.2017.01.054

Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., Sutton, D. J. (2012) Heavy metals toxicity and the environment, EXS, 101:133–164

Thomsen, P. T. (2015) Short communication: Efficacy of copper sulfate hoof baths against digital dermatitis—Where is the evidence?, J. Dairy Sci., 98:2539-2544

Tsai, A., Uemura, S., Johansson, M., Puglisi, E., Marshall, R., Colin, C., E., Korlach, J., Ehrenberg, M., Puglisi, D. J (2013) The impact of aminoglycosides on the dynamics of translation elongation, Cell Rep., 3(2):497–508

Ţugui, C.G., Vlădăreanu, I., Baricz, A., Coman, C. (2015) Detection of beta-lactamase resistance genes in a hospital chlorinated wastewater treatment system. Studia UBB Biologia, 60:33-38

Underwood, E. J., Suttle, N. F. (1999) Zinc. In: Mineral nutrition of livestock. 3rd ed. CAB International New York, 477–512

Voica, D. M., Bartha, L., Banciu, H. K., Oren, A. (2016) Heavy metal resistance in halophilic Bacteria and Archaea, FEMS Microbiol. Lett., 363(14):1-9

Wales, D. A., Davies, R. H. (2015) Co-Selection of Resistance to Antibiotics, Biocides and Heavy Metals, and Its Relevance to Foodborne Pathogens, Antibiotics (Basel), 4(4): 567–604

Walker, B., Barrett, S., Polasky, S. Galaz, V., Folke, C., Engström, G., Daily, G. (2009) Looming global-scale failures and missing institutions, Science, 325:1345-1346

Webber, M. A., Piddock, L. J. V. (2013) The importance of efflux pumps in bacterial antibiotic resistance, J. Antimicrob. Chemother., 51(1):9-11

Wireman, J., Liebert, C. A., Smith, T., Summers, A. O. (1997) Association of mercury resistance with antibiotic resistance in the gram-negative fecal bacteria of primates, Appl Environ Microbiol., 63(11):4494–4503

Wright, G. D. (2007) The antibiotic resistome: the nexus of chemical and genetic diversity, Nature Revs. Microbiol., 5:175-186

Wright, G. D., Poinar, H. (2012) Antibiotic resistance is ancient: implications for drug discovery, Trends Microbiol., 20:157-159

Wu, X. Y., Yang, Y. F. (2011) Heavy metal (Pb, Co, Cd, Cr, Cu, Fe, Mn and Zn) concentrations in harvest-size white shrimp Litopenaeus vannamei tissues from aquaculture and wild source, J. Food Comp. Anal., 24:62-65

Yazdankhah, S., Rudi, K., Bernhoft, A. (2014) Zinc and copper in animal feed – development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin, Microb. Ecol. Health Dis., 25:10

Zhang, F., Li, Y., Yang, M., Li, W. (2012) Content of Heavy Metals in Animal Feeds and Manures from Farms of Different Scales in Northeast China, Int. J. Environ. Res. Public Health, 9:2658-2668

Zhang, W., Ki, J. S., Qian P. Y. (2008) Microbial diversity in polluted harbor sediments I: bacterial community assessment based on four clone libraries of 16S rDNA, Estuar. Coast. Shelf. Sci. 76:668–681

Published

2017-06-20

Issue

Section

Review