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Water environments: metal-tolerant and antibiotic-resistant bacteria

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Abstract

The potential threat of both metals and antibiotics to the environment and human health has raised significant concerns in the last decade. Metal-resistant and antibiotic-resistant bacteria are found in most environments, including water, and the risk posed to humans and animals due to the spread of antibiotic-resistant bacteria and antibiotic-resistant genes in the environment is increasing. Bacteria have developed the ability to tolerate metals even at notable concentrations. This ability tends to favor the selection of antibiotic-resistant strains, even in pristine water environments, with the potential risk of spreading this resistance to human pathogens. In this mini-review, we focus on investigations performed in marine and freshwater environments worldwide, highlighting the presence of co-resistance to metals and antibiotics.

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References

  • Al-Musharafi, S. K., Mahmoud, I. Y., & Al-Bahry, S. N. (2015). Heavy metals and antibiotic resistant bacteria in green turtles are indicators of environmental pollution. International Journal of Environmental and Ecological Engineering, 9(4), 356–359.

    Google Scholar 

  • Acharya, K.P. and Wilson, R.T. (2019) Antimicrobial Resistance in Nepal. Frontiers Medicine, 6, 105. https://doi.org/10.3389/fmed.2019.00105.

  • Arias-Andres, M., Klumper, U., Rojas-Jimenez, K., & Grossart, H.-P. (2018). Microplastic pollution increases gene exchange in aquatic ecosystems. Environmental Pollution, 237, 253–261.

    CAS  Google Scholar 

  • Baker-Austin, C., Wright, M. S., Stepanauskas, R., & McArthur, J. V. (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(1), 176–182.

    CAS  Google Scholar 

  • Baquero, F., Martínez, J. L., & Cantó, R. (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19, 260–265.

    CAS  Google Scholar 

  • Barbieri, P., Galassi, G., & Galli, E. (1998). Plasmid-encoded mercury resistance in a Pseudomonas stutzeri strain that degrades o-xylene. FEMS Microbiology Ecology, 20, 185–194.

    Google Scholar 

  • Berg, J., Thorsen, M. K., Holm, P. E., Jensen, J., Nybroe, O., & Brandt, K. K. (2010). Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environmental Science and Technology, 44, 8724–8728.

    CAS  Google Scholar 

  • Burridge, L., Weis, J. S., Cabello, F., Pizarro, J., and Bostick, K. (2010). Chemical use in salmon aquaculture: a review of current practices and possible environmental effects. Aquaculture 306, 7–23.

  • Calomiris, J., Armstrong, L. J., & Seilde, R. (1984). Association of metal tolerance with multiple antibiotic resistance of bacteria isolated from drinking water. Applied Environmental Microbiology, 48, 1238–1242.

    Google Scholar 

  • Canstein, V. H., Li, Y., Timmis, K. N., Deckwer, W. D., & Wagner-Dobler, I. (1999). Removal of mercury from chloralkali electrolysis wastewater by a mercury-resistant Pseudomonas putida strain. Applied Environmental Microbiology, 65, 5279–5284.

    Google Scholar 

  • Chan, K. Y., & Dean, A. C. R. (1988). Effects of cadmium and lead on growth, respiration and enzyme activity of the marine bacterium Pseudomonas marina. Chemosphere, 17, 597–607.

    CAS  Google Scholar 

  • Chapman, J. S. (2003). Disinfectant resistance mechanisms, cross-resistance, co-resistance. International Biodeterioration & Biodegradation, 51(4), 271–276.

    CAS  Google Scholar 

  • Cycon, M., Mrozik, A., Piotrowska-Seget, Z. (2019) Antibiotics in the Soil Environment—Degradation and Their Impact on Microbial Activity and Diversity. Frontiers Microbiology, 10, 338. https://doi.org/10.3389/fmicb.2019.00338.

  • De Souza, M., Nair, S., Loka Bharathi, P. A., & Chandramohan, D. (2006). Metal and antibiotic-resistance in psychotropic bacteria from Antarctic marine waters. Ecotoxicology, 15, 379–384.

    Google Scholar 

  • Di Cesare, A., Eckert, E. M., Teruggi, A., Fontaneto, D., Bertoni, R., Callieri, C., & Corno, G. (2015). Constitutive presence of antibiotic resistance genes within the bacterial community of a large subalpine lake. Molecular Ecology, 24, 3888–3900.

    Google Scholar 

  • Farias, P. G., Espírito Santo, C., Branco, R., Francisco, R., Santos, S., Hansen, L., Sorensen, S., & Moraisa, P. V. (2015). Natural hot spots for gain of multiple resistances: arsenic and antibiotic resistances in heterotrophic, aerobic Bacteria from marine hydrothermal vent fields. Applied Environmental Microbiology, 7, 2534–2543.

    Google Scholar 

  • Fernández-Calviño D &, Bååth, E. (2013). Co-selection for antibiotic tolerance in Cu-polluted soil is detected at higher Cu-concentrations than increased Cu-tolerance. Soil Biology and Biochemistry, 57, 953–956.

  • Flach, C. F., Pal, C., Svensson, C. J., Kristiansson, E., Östman, M., Bengtsson-Palme, J., Tysklind, M., & Joakim Larsson, D. G. (2017). Does antifouling paint select for antibiotic resistance? The Science of the Total Environment, 461–468.

  • Forsberg, K. J., Reyes, A., Wang, B., Selleck, E.M., Sommer, M.O. &, Dantas, G. (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337(6098),1107–1111.

  • Gillings, M. R., Gaze, W. H., Pruden, A., Smalla, K., Tiedje, J. M., & Zhu, Y.-G. (2015). Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. The ISME Journal, 9, 1269–1279.

    CAS  Google Scholar 

  • Gillings, M., Boucher, Y., Labbate, M., Holmes, A., Krishnan, S., Holley, M., et al. (2008). The evolution of class 1 integrons and the rise of antibiotic resistance. Journal of Bacteriology, 190, 5095–5100.

  • Gonzàles-Aravena, M., Urtubia, R., Del Campo, K., Lavìn, P., Wong, C. M. V. L., Càrdenas, C. A., & Gonzàles-Rocha, G. (2016). Antibiotic and metal resistance of cultivable bacteria in the Antarctic Sea urchin. Antarctic Science, 1–8.

  • Guo, X., Chen, C., & Wang, J. (2019). Sorption of sulfamethoxazole onto six types of microplastics. Chemosphere, 228, 300–308. https://doi.org/10.1016/j.chemosphere.

    Article  CAS  Google Scholar 

  • Hacioglu, N., & Tosunoglu, M. (2014). Determination of antimicrobial and heavy metal resistance profiles of some bacteria isolated from aquatic amphibian and reptile species. Environmental Monitoring and Assessment, 186, 407–413.

    CAS  Google Scholar 

  • Han, F. X., Banin, A., Su, Y., Monts, D. L., Plodinec, J. M., Kingery, W. L., & Triplett, G. E. (2002). Industrial age anthropogenic inputs of heavy metals into the pedosphere. Naturwissenschaften, 89, 497–504.

    CAS  Google Scholar 

  • Hatosy, S. M., & Martiny, A. C. (2015). The ocean as a global reservoir of antibiotic resistance genes. Applied Environmental Microbiology, 81(21), 7593–7599.

    CAS  Google Scholar 

  • Hu, Q., & Chen, L. (2016). Virulence and antibiotic and heavy metal resistance of Vibrio parahaemolyticus isolated from crustaceans and shellfish in Shanghai, China. Journal of Food Protection, 79(8), 1371–1377.

    CAS  Google Scholar 

  • Huang, Y., Zhang, L., Tiu, L., & Wang, H. H. (2015). Characterization of antibiotic resistance in commensal bacteria from an aquaculture ecosystem. Frontiers in Microbiology, 6, 914.

    Google Scholar 

  • Imran, M., Das, K. R., & Naik, M. M. (2019). Co-selection of multi-antibiotic resistance in bacterial pathogens in metal and microplastic contaminated environments: an emerging health threat. Chemosphere, 215, 846–857.

    CAS  Google Scholar 

  • Jenkins, D. J., & Stekel, D. J. (2010). De novo evolution of complex, global and hierarchical gene regulatory mechanisms. Journal of Molecular Evolution, 71(2), 128–140.

    CAS  Google Scholar 

  • Kang, C., & So, J. (2016). Antibiotic and heavy metal resistance in Shewanella putrefaciens strains isolated from shellfishes collected from West Sea, Korea. Marine Pollution Bulletin, 112, 111–116.

    CAS  Google Scholar 

  • Keswani, A., Oliver, D. M., Gutierrez, T., & Quilliam, R. S. (2016). Microbial hitchhikers on marine plastic debris: human exposure risks at bathing waters and beach environments. Marine Environmental Research, 118, 10–19.

    CAS  Google Scholar 

  • Kholodii, G., Mindlin, S., Petrova, M., & Minakhina, S. (2003). Tn5060 from the Siberian permafrost is most closely related to the ancestor of Tn21 prior to integron acquisition. FEMS Microbiology Letters, 226(2), 251–255.

    CAS  Google Scholar 

  • Kimiran-Erdem, A., Arslan, E. O., Sanli Yurudu, N. O., Zeybek, Z., Dogruoz, N., & Cotuk, A. (2007). Isolation and identification of enterococci from seawater samples: assessment of their resistance to antibiotics and heavy metals. Environmental Monitoring and Assessment, 125(1–3), 219–228.

    CAS  Google Scholar 

  • Kimiran-Erdem, A., Arslan-Aydoğdu, E. O., Gürün, S., & Altun, O. (2015). Determination of multiple antibiotic and heavy metal resistance of the bacteria isolated from the Küçükçekmece Lagoon, Turkey. Polish Journal of Environmental Studies 24(3), 1077–1084.

  • Koditschek, L. K., & Guyre, P. (1974). Resistance transfer fecal coliforms isolated from the Whippany River. Water Research, 8, 747–752.

    Google Scholar 

  • Kraemer, S.A., Ramachandran, A., Perron, G.G. (2019). Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy. Microorganisms, 7, 180. https://doi.org/10.3390/microorganisms7060180.

  • Laganà, P., Caruso, G., Corsi, I., Bergami, E., Venuti, V., Majolino, D., La Ferla, R., Azzaro, M., & Cappello, S. (2019). Do plastics serve as a possible vector for the spread of antibiotic resistance? First insights from bacteria associated to a polystyrene piece from King George Island (Antarctica). International. Journal of Hygiene and Environmental Health, 222, 89–100.

    Google Scholar 

  • Lee, S. W., Najiah, M., Wendy, W., Zahrol, A., & Nadirah, M. (2009). Multiple antibiotic resistance and heavy metal resistance profile of bacteria isolated from giant freshwater prawn (Macrobrachium rosenbergii) hatchery. Agricultural Sciences in China, 8(6), 740–745.

    CAS  Google Scholar 

  • Li, J., Zhang, K., & Zhang, H. (2018). Adsorption of antibiotics on microplastics. Environmental Pollution, 237, 460–467. https://doi.org/10.1016/j.envpol.2018.02.050.

    Article  CAS  Google Scholar 

  • Lin, J., Nishino, K., Roberts, M. C., Tolmasky, M., Aminov, R. I., & Zhang, L. (2015). Mechanisms of antibiotics resistance. Frontiers in Microbiology, 6(34), 1–3.

  • Mangano, S., Michaud, L., Caruso, C., & Lo Giudice, A. (2014). Metal and antibiotic resistance in psychotropic bacteria associated with the Antarctic sponge Hemigellius pilosus (Kirkpatrick, 1907). Polar Biology, 37, 227–235.

    Google Scholar 

  • Marinescu, F., Chifiriuc, M. C., Măruțescu, L., Ilie, M., Savin, I., Anghel, A., Marcuș, I., Tociu, C., & Marcu, E. (2017). Prevalence of heavy metal and antibiotic resistance in bacterial isolates from wastewater and receiving aquatic environments. Biointerface Research in Applied Chemistry, 7(5), 2140–2144.

    CAS  Google Scholar 

  • Martinez, J. L., Coque, T. M., & Baquero, F. (2009). What is a resistance gene? Ranking risk in resistomes. Nature Review Microbiology, 13(2), 116–123.

    Google Scholar 

  • Miranda, C. D., & Castillo, G. (1998). Resistance to antibiotic and heavy metals of motile aeromonads from Chilean freshwater. The Science of the Total Environment, 224, 167–176.

    CAS  Google Scholar 

  • Nair, S., Chandramohan, D., & Loka Bharathi, P. A. (1992). Differential sensitivity of pigmented and non-pigmented marine bacteria to metals and antibiotics. Water Research, 26(4), 431–434.

    CAS  Google Scholar 

  • Najiah, M., Lee, S. W., Wendy, W., Teel, L. W., Nadirah, M., & Faizah, S. H. (2009). Antibiotic resistance and heavy metals tolerance in gram-negative bacteria from diseased American bullfrog (Rana catesbeiana) cultured in Malaysia. Agricultural Science in China, 8(10), 1270–1275.

    Google Scholar 

  • Nicholson, F. A., Smith, S. R., Alloway, B. J., Carlton-Smith, C., & Chambers, B. J. (2003). An inventory of heavy metals inputs to agricultural soils in England and Wales. Science of the Total Environment, 311, 205–219.

  • NOAA, 2009. NOAA technical memorandum NOS-OR&R-30. In: Arthur, C., Baker, J., Bamford, H. (Eds.), Proceedings of the International Research Workshop on the Occurrence, Effects, and Fate of Microplastic Marine Debris, Tacoma, WA, Sept 9-11, 2008. NOAA: Silver Spring, MD.

  • O’Donovan, S.O., Mestre, M.C., Abel, S., Fonseca, T.G., Carteny, C.C., Cormier, B., Keiter, S.H., Bebianno, M.J. (2018). Ecotoxicological effects of chemical contaminants adsorbed to microplastics in the clam Scrobicularia plana. Frontiers in Marine Science,143.

  • Pagano, G., Aliberti, F., Guida, M., Oral, R., Siciliano, A., Trifuoggi, M., & Tommasi, F. (2015). Rare earth elements in human and animal health: state of art and research priorities. Environmental Research, 142, 215–220.

    CAS  Google Scholar 

  • Pal, C., Asiani, K., Arya, S., Rensing, C., Stekel, D. J., Larsson, D. G. J., & Hobman, J. L. (2017). Metal resistance and its association with antibiotic resistance. Advances in Microbial Physiology, 216–314.

  • Perry, J., Waglechner, N., & Wright, G. (2016). The prehistory of antibiotic resistance. Cold Spring Harbor Perspectives in Medicine, 6(6), a025197.

    Google Scholar 

  • Rahman, Z., & Sing, V. P. (2018). Assessment of heavy metal contamination and Hg-resistant bacteria in surface water from different regions of Delhi, India. Saudi Journal of Biological Sciences, 25, 1687–1695.

    CAS  Google Scholar 

  • Revel, M., Châtel, A., & Mouneyrac, C. (2018). Micro(nano)plastics: A threat to human health? Current. Opinion. Environmental Science and. Health, 1, 17–23.

    Google Scholar 

  • 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. Journal of Applied Microbiology, 82, 245–252.

    CAS  Google Scholar 

  • Seiler, C., & Berendonk, T. U. (2012). Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Frontiers in Microbiology, 3(399), 1–10.

    Google Scholar 

  • Stepanauskas, R., Glenn, T. C., Jagoe, C. H., Tuckfield, R. C., Lindell, A. H., King, C. J., & Mc Arthur, J. V. (2006). Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environmental Microbiology, 8(9), 1510–1514.

    CAS  Google Scholar 

  • Stokes, H. W., Nesbo, C. L., Holley, M., Bahl, M. I., Gillings, M. R., & Boucher, Y. (2006). Class 1 integrons potentially predating the association with Tn402-like transposition genes are present in a sediment microbial community. Journal of Bacteriology., 188, 5722–5730.

    CAS  Google Scholar 

  • Summers, A.O., Wireman, J., Vimy, M.J., Lorscheider, F.L., Marshall, B., Levy, S.B., Bennett, S.B.S., Billard, L. 1993. Mercury released from dental ‘silver’ fillings provokes an increase in mercury- and antibiotic-resistant bacteria in oral and intestinal floras of primates. Antimicrobial Agents and Chemotheraphy, 37, 825–834.

  • Suzuki, S., Kimura, M., Agusa, T., & Rahman, H. M. (2012). Vanadium accelerates horizontal transfer of tet(M) gene from marine Photobacterium to Escherichia coli. FEMS Microbiology Letters, 336, 52–56.

    CAS  Google Scholar 

  • Suzuki, S., Pruden, A., Virta, M., Zhang, T. (2017) Editorial: Antibiotic Resistance in Aquatic Systems. Frontiers Microbiology, 8(14), 1–3. https://doi.org/10.3389/fmicb.2017.00014.

  • Tazzyman, S. J., & Bonhoeffer, S. (2014). Why there are no essential genes on plasmids. Molecular Biology and Evolution, 32, 3079–3088.

    Google Scholar 

  • Vignaroli., C., Pasquaroli, S., Citterio, C., Di Cesare, A., Mangiaterra, G., Fattorini, D., & Biavasco, F. (2018). Antibiotic and heavy metal resistance in enterococci from coastal marine sediment. Environmental Pollution, 237, 406–413.

  • 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. Applied Environmental Microbiology, 63(11), 4494–4503.

    CAS  Google Scholar 

  • Wright, S. L., Thompson, R. C. & Galloway, T. S. (2013) ‘The physical impacts of microplastics on marine organisms: A review’. Environmental Pollution, 178, 483–492.

  • Zhang, M., Wan, K., Zeng, J., Lin, W., Ye, C., Yu X. (2020). Co-selection and stability of bacterial antibiotic resistance by arsenic pollution accidents in source water. Environment International, 105351.

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Acknowledgments

The author wishes to thank the two reviewers who greatly improved the manuscript quality. Thanks to Filippo Brusco for helping to design graphs.

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  1. Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154, Torino, Italy

    Stefania Squadrone

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Squadrone, S. Water environments: metal-tolerant and antibiotic-resistant bacteria. Environ Monit Assess 192, 238 (2020). https://doi.org/10.1007/s10661-020-8191-8

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