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Insights to antimicrobial resistance: heavy metals can inhibit antibiotic resistance in bacteria isolated from wastewater

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Abstract

The alarming upsurge in the co-existence of heavy metal and antibiotic resistance may have a devastating impact on humans, animals, and the environment. Four metal-resistant bacteria were isolated from hospital effluents and industrial drain. Heavy metal resistance and antimicrobial resistance were examined in the isolates followed by identification through 16S rRNA gene sequencing. Delftia tsuruhatensis strain FK-01 and Carnobacterium inhibens strain FK-02 tolerated arsenic with maximal tolerated concentration (MTC) of 30 mM and 10 mM, respectively. Staphylococcus hominis strain FK-04 tolerated copper up to 4 mM and lead-resistant Raoultella ornithinolytica strain FK-05 exhibited tolerance to 1 mM lead. The growth kinetics of bacteria were monitored in the presence of metals and the following antibiotics, tetracycline, chloramphenicol, and kanamycin. The presence of arsenate significantly enhanced tetracycline resistance in C. inhibens. Heavy metal–induced antibiotic resistance was also observed in S. hominis and R. ornithinolytica, against chloramphenicol and tetracycline respectively. D. tsuruhatensis showed resistance to kanamycin but when grown in the presence of arsenic and kanamycin, bacteria lost resistance to the antibiotic. Therefore, it is suggested that the novel arsenate-resistant strain Delftia tsuruhatensis FK-01 has a unique ability to inhibit antimicrobial resistance that can be harnessed in bioremediation.

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References

  • Ahmed, N. H., Baruah, F. K., & Grover, R. K. (2017). Staphylococcus hominis subsp. novobiosepticus, an emerging multidrug-resistant bacterium, as a causative agent of septicaemia in cancer patients. Indian Journal of Medical Research, 146(3), 420–425. https://doi.org/10.4103/ijmr.IJMR_1362_15

    Article  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(4), 176–182. https://doi.org/10.1016/j.tim.2006.02.006

    Article  CAS  Google Scholar 

  • Ballash, G. A., Albers, A. L., Mollenkopf, D. F., Sechrist, E., Adams, R. J., & Wittum, T. E. (2021). Antimicrobial resistant bacteria recovered from retail ground meat products in the US include a Raoultella ornithinolytica co-harboring blaKPC-2 and blaNDM-5. Scientific Reports, 11(1), 1–12.

    Article  Google Scholar 

  • Berg, J., Tom-Petersen, A., & Nybroe, O. (2005). Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Letters in Applied Microbiology, 40(2), 146–151. https://doi.org/10.1111/j.1472-765X.2004.01650.x

    Article  CAS  Google Scholar 

  • Biswas, R., Halder, U., Kabiraj, A., Mondal, A., & Bandopadhyay, R. (2021). Overview on the role of heavy metals tolerance on developing antibiotic resistance in both Gram-negative and Gram-positive bacteria. Archives of Microbiology, 203, 2761–2770.

    Article  CAS  Google Scholar 

  • Chen, S., Li, X., Sun, G., Zhang, Y., Su, J., & Ye, J. (2015). Heavy metal induced antibiotic resistance in bacterium LSJC7. International Journal of Molecular Sciences, 16(10), 23390–23404. https://doi.org/10.3390/ijms161023390

    Article  CAS  Google Scholar 

  • Cheng, C., Zhou, W., Dong, X., Zhang, P., Zhou, K., Zhou, D., & Ying, J. (2021). Genomic analysis of Delftia tsuruhatensis strain TR1180 isolated from a patient from China with In4-like integron-associated antimicrobial resistance. Frontiers in Cellular and Infection Microbiology, 11, 663933. https://doi.org/10.3389/fcimb.2021.663933

    Article  CAS  Google Scholar 

  • Cho, S. M., Hong, S. G., Lee, Y., Song, W., Yong, D., Jeong, S. H., & Chong, Y. (2021). First identification of IMP-1 metallo-β-lactamase in Delftia tsuruhatensis strain CRS1243 isolated from a clinical specimen. Annals of Laboratory Medicine, 41(4), 436–438.

    Article  Google Scholar 

  • De La Rosa-Acosta, M., Jiménez-Collazo, J., Maldonado-Román, M., Malavé-Llamas, K., & Carlos Musa-Wasil, J. (2016). Bacteria as potential indicators of heavy metal contamination in a tropical mangrove and the implications on environmental and human health. Journal of Tropical Life Science, 5(3), 100–116. https://doi.org/10.11594/jtls.05.03.01

  • El-Shannat, S. M., Abd El-Tawab, A. A., & Hassan, W. M. (2020). Emergence of Raoultella ornithinolytica isolated from chicken products in Alexandria, Egypt. Veterinary World, 13(7), 1473.

    Article  CAS  Google Scholar 

  • Emmanuel, E., Perrodin, Y., Keck, G., Blanchard, J. M., & Vermande, P. (2002). Effects of hospital wastewater on aquatic ecosystem. In Proceedings of the XXVIII Congreso Interamericano de Ingenieria Sanitaria y Ambiental. Cancun, México (pp. 27–31).

  • Ghernaout, D., & Elboughdiri, N. (2020). Antibiotics resistance in water mediums: Background, facts, and trends. Applied Engineering, 4(1), 1–6.

    Google Scholar 

  • Hajjar, R., Ambaraghassi, G., Sebajang, H., Schwenter, F., & Su, S. H. (2020). Raoultella ornithinolytica: Emergence and resistance. Infection and Drug Resistance, 13, 1091–1104.

    Article  Google Scholar 

  • Jin, Y., Wu, S., Zeng, Z., & Fu, Z. (2017). Effects of environmental pollutants on gut microbiota. Environmental Pollution, 222, 1–9.

    Article  CAS  Google Scholar 

  • Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., & Madden, T. L. (2008). NCBI BLAST: A better web interface. Nucleic Acids Research, 36(Web Server issue), W5–W9. https://doi.org/10.1093/nar/gkn201

    Article  CAS  Google Scholar 

  • Khan, G. A., Berglund, B., Khan, K. M., Lindgren, P. E., & Fick, J. (2013). Occurrence and abundance of antibiotics and resistance genes in rivers, canal and near drug formulation facilities - A study in Pakistan. PLoS One, 8(6), 4–11. https://doi.org/10.1371/journal.pone.0062712

    Article  CAS  Google Scholar 

  • Koc, S., Kabatas, B., & Icgen, B. (2013). Multidrug and heavy metal-resistant Raoultella planticola isolated from surface water. Bulletin of Environmental Contamination and Toxicology, 91(2), 177–183. https://doi.org/10.1007/s00128-013-1031-6

    Article  CAS  Google Scholar 

  • Kristiansen, M., Merrifield, D. L., Vecino, J. L. G., Myklebust, R., & Ringø, E. (2011). Evaluation of prebiotic and probiotic effects on the intestinal gut microbiota and histology of Atlantic salmon (Salmo salar L.). Journal of Aquaculture Research and Development, S1, 009. https://doi.org/10.4172/2155-9546.S1-009

    Article  Google Scholar 

  • Lawal, O. U., Fraqueza, M. J., Worning, P., Bouchami, O., Bartels, M. D., Goncalves, L., & Miragaia, M. (2021). Staphylococcus saprophyticus causing infections in humans are associated with high resistance to heavy metals. Antimicrobial Agents and Chemotherapy, 65, e02685-e2720. https://doi.org/10.1128/AAC.02685-20

    Article  CAS  Google Scholar 

  • Leisner, J. J., Laursen, B. G., Prévost, H., Drider, D., & Dalgaard, P. (2007). Carnobacterium: Positive and negative effects in the environment and in foods. FEMS Microbiology Reviews, 31(5), 592–613. https://doi.org/10.1111/j.1574-6976.2007.00080.x

    Article  CAS  Google Scholar 

  • Li, B., & Webster, T. J. (2018). Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections. Journal of Orthopaedic Research, 36(1), 22–32. https://doi.org/10.1002/jor.23656

    Article  Google Scholar 

  • Li, H., Liu, H., Zeng, Q., Xu, M., Li, Y., Wang, W., & Zhong, Y. (2020). Isolation and appraisal of a non-fermentative bacterium, Delftia tsuruhatensis, as denitrifying phosphate-accumulating organism and optimal growth conditions. Journal of Water Process Engineering, 36, 101296.

    Article  Google Scholar 

  • Lin, Y. -F., Yang, J., & Rosen, B. P. (2007). ArsD residues Cys12, Cys13, and Cys18 form an As(III)-binding site required for arsenic metallochaperone activity. Journal of Biological Chemistry, 282(23), 16783–16791. https://doi.org/10.1074/jbc.M700886200

    Article  CAS  Google Scholar 

  • Lo, C. K. L., & Sheth, P. M. (2021). Carnobacterium inhibens isolated in blood culture of an immunocompromised, metastatic cancer patient: A case report and literature review. BMC Infectious Diseases, 21(1), 1–5.

    Article  Google Scholar 

  • Lu, L., Liu, J., Li, Z., Zou, X., Guo, J., Liu, Z., & Zhou, Y. (2020). Antibiotic resistance gene abundances associated with heavy metals and antibiotics in the sediments of Changshou Lake in the three Gorges Reservoir area, China. Ecological Indicators, 113, 106275.

    Article  CAS  Google Scholar 

  • Lucious, S., Reddy, E. A., Anuradha, V., Vijaya, P. P., Ali, M., Nagarajan, Y., & Parveen, P. K. (2013). Heavy metal tolerance and antibiotic sensitivity of bacterial strains isolated from tannery effluent. Asian Journal of Experimental Biological Sciences, 4, 597–606.

    Google Scholar 

  • Mal, P. B., Sarfaraz, S., Herekar, F., & Ambreen, R. (2019). Clinical manifestation and outcomes of multi-drug resistant (MDR) Raoultella terrigena infection – A case series at Indus Health Network, Karachi, Pakistan. Idcases. https://doi.org/10.1016/j.idcr.2019.e00628

    Article  Google Scholar 

  • Manske, M. (2006). GENtle, a free multi-purpose molecular biology tool (Doctoral dissertation, Universität zu Köln).

  • Martinez, J. L. (2009). Environmental pollution by antibiotics and by antibiotic resistance determinants. Environmental Pollution, 157(11), 2893–2902. https://doi.org/10.1016/j.envpol.2009.05.051

    Article  CAS  Google Scholar 

  • Martinez, J. L., & Rojo, F. (2011). Metabolic regulation of antibiotic resistance. FEMS Microbiology Reviews, 35(5), 768–789. https://doi.org/10.1111/j.1574-6976.2011.00282.x

    Article  CAS  Google Scholar 

  • Mazhar, S. H., Li, X., Rashid, A., Su, J., Xu, J., Brejnrod, A. D., & Rensing, C. (2021). Co-selection of antibiotic resistance genes, and mobile genetic elements in the presence of heavy metals in poultry farm environments. Science of the Total Environment, 755, 142702.

    Article  CAS  Google Scholar 

  • Mokarram, M., Saber, A., & Sheykhi, V. (2020). Effects of heavy metal contamination on river water quality due to release of industrial effluents. Journal of Cleaner Production, 277, 123380.

    Article  CAS  Google Scholar 

  • Nicholson, W. L., Krivushin, K., Gilichinsky, D., & Schuerger, A. C. (2013). Growth of Carnobacterium spp. from permafrost under low pressure, temperature, and anoxic atmosphere has implications for Earth microbes on Mars. Proceedings of the National Academy of Sciences, 110(2), 666–671.

    Article  CAS  Google Scholar 

  • Nikolaou, A., Meric, S., & Fatta, D. (2007). Occurrence patterns of pharmaceuticals in water and wastewater environments. Analytical and Bioanalytical Chemistry, 387(4), 1225–1234. https://doi.org/10.1007/s00216-006-1035-8

    Article  CAS  Google Scholar 

  • Palazzo, I. C. V., d’Azevedo, P. A., Secchi, C., Pignatari, A. C. C., & da Costa Darini, A. L. (2008). Staphylococcus hominis subsp. novobiosepticus strains causing nosocomial bloodstream infection in Brazil. Journal of Antimicrobial Chemotherapy, 62(6), 1222–1226. https://doi.org/10.1093/jac/dkn375

    Article  CAS  Google Scholar 

  • Pas, M. L., Vanneste, K., Bokma, J., Van Driessche, L., De Keersmaecker, S. C., Roosens, N. H., & Pardon, B. (2021). Case report: Multidrug resistant Raoultella ornithinolytica in a septicemic calf. Frontiers in Veterinary Science, 8, 278.

    Article  Google Scholar 

  • Peltier, E., Vincent, J., Finn, C., & Graham, D. W. (2010). Zinc-induced antibiotic resistance in activated sludge bioreactors. Water Research, 44(13), 3829–3836. https://doi.org/10.1016/j.watres.2010.04.041

    Article  CAS  Google Scholar 

  • Qiao, L. D., Chen, S., Yang, Y., Zhang, K., Zheng, B., Guo, H. F., & Tian, Y. (2013). Characteristics of urinary tract infection pathogens and their in vitro susceptibility to antimicrobial agents in China: Data from a multicenter study. British Medical Journal Open, 3(12), e004152. https://doi.org/10.1136/bmjopen-2013-004152

    Article  Google Scholar 

  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(Database issue), D590–D596. https://doi.org/10.1093/nar/gks1219-

    Article  CAS  Google Scholar 

  • Ringø, E. (2004). Lactic acid bacteria in fish and fish farming. In Lactic Acid Bacteria Microbiological and Functional Aspects, Third Edition: Revised and Expanded. https://doi.org/10.1201/9780824752033.ch21

  • Ringø, E. (2008). The ability of carnobacteria isolated from fish intestine to inhibit growth of fish pathogenic bacteria: A screening study. Aquaculture Research, 39(2), 171–180. https://doi.org/10.1111/j.1365-2109.2007.01876.x

    Article  CAS  Google Scholar 

  • Romaniuk, K., Ciok, A., Decewicz, P., Uhrynowski, W., Budzik, K., Nieckarz, M., & Dziewit, L. (2018). Insight into heavy metal resistome of soil psychrotolerant bacteria originating from King George Island (Antarctica). Polar Biology, 41(7), 1319–1333.

    Article  Google Scholar 

  • Roy, P., Ahmed, N. H., Biswal, I., & Grover, R. K. (2014). Multidrug-resistant Staphylococcus hominis subsp. novobiosepticus causing septicemia in patients with malignancy. Indian Journal of Pathology and Microbiology, 57(2), 275–277.

    Article  Google Scholar 

  • Samanta, A., Bera, P., Khatun, M., Sinha, C., Pal, P., Lalee, A., & Mandal, A. (2012). An investigation on heavy metal tolerance and antibiotic resistance properties of bacterial strain Bacillus sp. isolated from municipal waste. Journal of Microbiology and Biotechnology Research, 2(1), 178–189.

    CAS  Google Scholar 

  • Schmidt, T., & Schlegel, H. G. (1994). Combined nickel-cobalt-cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A. Journal of Bacteriology, 176(22), 7045–7054.

    Article  CAS  Google Scholar 

  • Segura, P. A., François, M., Gagnon, C., & Sauvé, S. (2009). Review of the occurrence of anti-infectives in contaminated wastewaters and natural and drinking waters. Environmental Health Perspectives, 117(5), 675–684. https://doi.org/10.1289/ehp.11776

    Article  CAS  Google Scholar 

  • Seng, P., Boushab, B. M., Romain, F., Gouriet, F., Bruder, N., Martin, C., & Stein, A. (2016). Emerging role of Raoultella ornithinolytica in human infections: A series of cases and review of the literature. International Journal of Infectious Diseases, 45, 65–71. https://doi.org/10.1016/j.ijid.2016.02.014

    Article  Google Scholar 

  • Shigematsu, T., Yumihara, K., Ueda, Y., Numaguchi, M., Morimura, S., & Kida, K. (2003). Delftia tsuruhatensis sp. nov., a terephthalate-assimilating bacterium isolated from activated sludge. International Journal of Systematic and Evolutionary Microbiology, 53(5), 1479–1483.

    Article  CAS  Google Scholar 

  • Singh, J., & Kalamdhad, A. S. (2011). Effects of heavy metals on soil, plants, human health and aquatic life. International Journal of Research in Chemistry and Environment, 1, 15–21.

    Google Scholar 

  • Skurnik, D., Ruimy, R., Ready, D., Ruppe, E., Bernède-Bauduin, C., Djossou, F., & Andremont, A. (2010). Is exposure to mercury a driving force for the carriage of antibiotic resistance genes?. Journal of Medical Microbiology, 59, 804–807. https://doi.org/10.1099/jmm.0.017665-0

    Article  CAS  Google Scholar 

  • 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. Environmental Microbiology, 8(9), 1510–1514. https://doi.org/10.1111/j.1462-2920.2006.01091.x

    Article  CAS  Google Scholar 

  • Tokar, E. J., Benbrahim-Tallaa, L., & Waalkes, M. P. (2011). Metal ions in human cancer development. Metal Ions in Life Sciences, 8, 375–401.

    CAS  Google Scholar 

  • Tóth, A. G., Csabai, I., Krikó, E., Tőzsér, D., Maróti, G., Patai, Á. V., & Solymosi, N. (2020). Antimicrobial resistance genes in raw milk for human consumption. Scientific Reports, 10(1), 1–7.

    Article  Google Scholar 

  • Ugur, A., & Ceylan, Ö. (2003). Occurrence of resistance to antibiotics, metals, and plasmids in clinical strains of Staphylococcus spp. Archives of Medical Research, 34(2), 130–136. https://doi.org/10.1016/S0188-4409(03)00006-7

    Article  CAS  Google Scholar 

  • Webber, M. A., & Piddock, L. J. V. (2003). The importance of efflux pumps in bacterial antibiotic resistance. Journal of Antimicrobial Chemotherapy, 51(1), 9–11. https://doi.org/10.1093/jac/dkg050

    Article  CAS  Google Scholar 

  • Wei, B., & Yang, L. (2010). A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchemical Journal, 94, 99–107. https://doi.org/10.1016/j.microc.2009.09.014

    Article  CAS  Google Scholar 

  • Zhou, Y., Xu, Y. B., Xu, J. X., Zhang, X. H., Xu, S. H., & Du, Q. P. (2015). Combined toxic effects of heavy metals and antibiotics on a Pseudomonas fluorescens strain ZY2 isolated from swine wastewater. International Journal of Molecular Sciences, 16(2), 2839–2850. https://doi.org/10.3390/ijms16022839

    Article  CAS  Google Scholar 

  • Zolgharnein, H., Lila, M., Azmi, M., Saad, M. Z., Rahim, A., Abd, C., & Mohamed, R. (2007). Detection of plasmids in heavy metal resistance bacteria isolated from the Persian Gulf and enclosed industrial areas. Iranian Journal of Biotechnology, 5(4), 232–239.

    CAS  Google Scholar 

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Acknowledgements

We are grateful to Dr Saad Imran Malik and Dr Ghulam Shabbir for their support in UV/VIS spectrophotometry experiments. We are also thankful to Dr. Abida Farooqi for her assistance in the experiments with AAS.

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  1. Functional Genomics Laboratory, Department of Biosciences, COMSATS University Islamabad, Islamabad, 45550, Pakistan

    Massab Bashir Khaira, Muhammad Bilal Yusuf & Fariha Khan

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FK, MBK, and MBY designed experiments. MBK and MBY collected samples and conducted experiments under the supervision of FK; MBK drafted the manuscripts; FK revised the manuscript.

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Correspondence to Fariha Khan.

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Khaira, M.B., Yusuf, M.B. & Khan, F. Insights to antimicrobial resistance: heavy metals can inhibit antibiotic resistance in bacteria isolated from wastewater. Environ Monit Assess 194, 252 (2022). https://doi.org/10.1007/s10661-022-09917-6

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