Metal Resistance in Bacteria from Contaminated Arctic Sediment is Driven by Metal Local Inputs

Abstract

Anthropogenic impact over the Pasvik River (Arctic Norway) is mainly caused by emissions from runoff from smelter and mine wastes, as well as by domestic sewage from the Russian, Norwegian, and Finnish settlements situated on its catchment area. In this study, sediment samples from sites within the Pasvik River area with different histories of metal input were analyzed for metal contamination and occurrence of metal-resistant bacteria in late spring and summer of 2014. The major differences in microbial and chemical parameters were mostly dependent on local inputs than seasonality. Higher concentrations of metals were generally detected in July rather than May, with inner stations that became particularly enriched in Cr, Ni, Cu, and Zn, but without significant differences. Bacterial resistance to metals, which resulted from viable counts on amended agar plates, was in the order Ni2+>Pb2+>Co2+>Zn2+>Cu2+>Cd2+>Hg2+, with higher values that were generally determined at inner stations. Among a total of 286 bacterial isolates (mainly achieved from Ni- and Pb-amended plates), the 7.2% showed multiresistance at increasing metal concentration (up to 10,000 ppm). Selected multiresistant isolates belonged to the genera Stenotrophomonas, Arthrobacter, and Serratia. Results highlighted that bacteria, rapidly responding to changing conditions, could be considered as true indicators of the harmful effect caused by contaminants on human health and environment and suggested their potential application in bioremediation processes of metal-polluted cold sites.

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References

  1. Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98:2243–2257

    Article  CAS  Google Scholar 

  2. Alboghobeish H, Tahmourespour A, Doudi M (2014) The study of Nickel Resistant Bacteria (NiRB) isolated from wastewaters polluted with different industrial sources. J Environ Health Sci Eng 12:44

    Article  CAS  Google Scholar 

  3. Ali M, Abdel-Satar A (2005) Studies of some heavy metals in water, sediment, fish and fish diets in some fish farms in El-Fayoum province. Egypt J Aquat Res 31:261–273

    Google Scholar 

  4. Altimira F, Yáñez C, Bravo G, González M, Rojas LA, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:193

    Article  CAS  Google Scholar 

  5. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  6. AMAP (2002) AMAP assessment: heavy metals in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo

    Google Scholar 

  7. AMAP (2011) AMAP assessment 2011: mercury in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway

  8. Amundsen P-A, Staldvik FJ, Lukin AA, Kashulin NA, Popova OA, Reshetnikov YS (1997) Heavy metal contamination in freshwater fish from the border region between Norway and Russia. Sci Total Environ 201:211–214

    Article  CAS  Google Scholar 

  9. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207

    Article  CAS  Google Scholar 

  10. Ceylan O, Ugur A (2012) Bio-monitoring of heavy metal resistance in Pseudomonas and Pseudomonas related genus. J Biol Environ Sci 6:233–242

    Google Scholar 

  11. Das S, Elavarasi A, Somasundharan PL, Khan SA (2009) Biosorption of heavy metals by marine bacteria: potential tool for detecting marine pollution. J Environ Health 9:38–43

    Google Scholar 

  12. Dauvalter V, Rognerud S (2001) Heavy metals pollution in sediments of the Pasvik River drainage. Chemosphere 42:9–18

    Article  CAS  Google Scholar 

  13. Ellis RJ, Neish B, Trett MW, Best JG, Weightman AJ, Morgan P, Fry JC (2001) Comparison of microbial and meiofaunal community analyses for determining impact of heavy metal contamination. J Microbiol Methodol 45:171–185

    Article  CAS  Google Scholar 

  14. Filali BK, Taoufik J, Zeroual Y, Dzairi FZ, Talbi M, Blaghen M (2000) Waste water bacterial isolates resistant to heavy metals and antibiotics. Curr Microbiol 41:151–156

    Article  CAS  Google Scholar 

  15. González-Aravena M, Urtubia R, Del Campo K, Lavín P, Wong CMVL, Cárdenas CA, González-Rocha G (2016) Antibiotic and metal resistance of cultivable bacteria in the Antarctic sea urchin. Antarct Sci 28:261–268

    Article  Google Scholar 

  16. Habi S, Daba H (2009) Plasmid incidence, antibiotic and metal resistance among enterobacteriaceae isolated from Algeria stream. Pak J Appl Sci 12:1474–1482

    CAS  Google Scholar 

  17. Laganà P, Votano L, Caruso G, Azzaro M, Lo Giudice A, Delia S (2018) Bacterial isolates from the Arctic region (Pasvik River, Norway): assessment of biofilm production and antibiotic susceptibility profiles. Environ Sci Pollut Res 25:1089–1102

    Article  CAS  Google Scholar 

  18. Lo Giudice A, Casella P, Bruni V, Michaud L (2013) Response of bacterial isolates from Antarctic shallow sediments towards heavy metals, antibiotics and polychlorinated biphenyls. Ecotoxicology 22:240–250

    Article  CAS  Google Scholar 

  19. Malik A, Khan IF, Aleem A (2002) Plasmid incidence in bacteria from agricultural and industrial soils. World J Microbiol Biotechnol 18:827–833

    Article  CAS  Google Scholar 

  20. Mangano S, Michaud L, Caruso C, Lo Giudice A (2014) Metal and antibiotic-resistance in psychrotrophic bacteria associated with the Antarctic sponge Hemigellius pilosus (Kirkpatrick, 1907). Polar Biol 37:227–235

    Article  Google Scholar 

  21. Michaud L, Di Cello F, Brilli M, Fani R, Lo Giudice A, Bruni V (2004) Biodiversity of cultivable psychrotrophic marine bacteria isolated from Terra Nova Bay (Ross Sea, Antarctica). FEMS Microbiol Lett 230:63–71

    Article  CAS  Google Scholar 

  22. Neethu CS, Mujeeb Rahiman KM, Saramma AV, Mohamed Hatha AA (2015) Heavy-metal resistance in Gram-negative bacteria isolated from Kongsfjord, Arctic. Can J Microbiol 61:429–435

    Article  CAS  Google Scholar 

  23. Nies DH (1999) Microbial heavy metals resistances. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  Google Scholar 

  24. Nies DH (2000) Heavy metal resistant bacteria as extremophiles: molecular physiology and biotechnological use of Ralstonia sp. CH34. Extremophiles 4:77–82

    Article  CAS  Google Scholar 

  25. Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228

    Article  CAS  Google Scholar 

  26. Pagès JM, James CE, Winterhalter M (2008) The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat Rev Microbiol 6:893–903

    Article  CAS  Google Scholar 

  27. Papale M, Conte A, Del Core M, Zito E, Sprovieri M, De Leo F, Rizzo C, Urzì C, De Domenico E, Luna GM, Michaud L, Lo Giudice A (2018) Heavy-metal resistant microorganisms in sediments from submarine canyons and the adjacent continental slope in the northeastern Ligurian margin (Western Mediterranean Sea). Prog Ocean 168:155–168

    Article  Google Scholar 

  28. Raja ECA, Selvam GS (2006) Isolation and characterization of a metalresistant Pseudomonas aeruginosa strain. World J Microbiol Biotechnol 22:577–586

    Article  CAS  Google Scholar 

  29. Rathnayake IVN, Megharaj M, Bolan N, Naidu R (2009) Tolerance of heavy metals by Gram positive soil bacteria. World Acad Sci Eng Technol 53:1185–1189

    Google Scholar 

  30. Selvin J, Shanmughapriya S, Gandhimathi R, Kiran GS, Ravji TR, Natarajaseenivasan K, Hema TA (2009) Optimization and production of novel antimicrobial agents from sponge associated marine actinomycetes Nocardiopsis dassonvillei MAD08. Appl Microbiol Biotechnol 83:435–445

    Article  CAS  Google Scholar 

  31. Sumampouw OJ, Risjani Y (2014) Bacteria as indicators of environmental pollution: review. Int J Ecosyst 4:251–258

    Google Scholar 

  32. Tada Y, Inoue T (2000) Use of oligotrophic bacteria for the biological monitoring of heavy metals. J Appl Microbiol 88:154–160

    Article  CAS  Google Scholar 

  33. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  34. Tomova I, Stoilova-Disheva M, Vasileva-Tonkova E (2014) Characterization of heavy metals resistant heterotrophic bacteria from soils in the Windmill Islands region, Wilkes Land, East Antarctica. Polish Pol Res 35:593–607

    Article  Google Scholar 

  35. Tomova I, Stoilova-Disheva M, Lazarkevich I, Vasileva-Tonkova E (2015) Antimicrobial activity and resistance to heavy metals and antibiotics of heterotrophic bacteria isolated from sediment and soil samples collected from two Antarctic islands. Front Life Sci 8:348–357

    Article  CAS  Google Scholar 

  36. Vaz-Moreira I, Nunes OC, Manaia CM (2011) Diversity and antibiotic resistance patterns of Sphingomonadaceae isolates from drinking water. Appl Environ Microbiol 77:5697–5706

    Article  CAS  Google Scholar 

  37. Zakaria ZA, Jaapar J, Ahmad WA (2004) Bacteria as bioindicators for metal contamination. In :Biomonitoring in tropical coastal ecosystems, Phang and Brown, 131–135

  38. Zampieri BDB, Bartelochi PA, Schultz L, de Oliveira MA, de Oliveira AJFD (2016) Diversity and distribution of heavy metal-resistant bacteria in polluted sediments of the Araça Bay, São Sebastião (SP), and the relationship between heavy metals and organic matter concentrations. Microb Ecol 72:582–594

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by grants from the INTERACT Transnational Access EU Program within the project SpongePOP “Sponge associated culturable microbiome able to degrade persistent organic pollutant along the Pasvik River and the Bokfjorden (Norway).” The authors thank the INTERACT coordinator Hannele Savela, and Lars Ola Nillson at the NIBIO Svanhovd Research Station (Svanvik, Pasvik Valley) for his continuous logistic support, which allowed us to perform successfully all of the lab and field work planned.

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Angelina Lo Giudice and Carmen Rizzo wrote the paper; Simona Caputo helped to write the paper and performed microbiological analyses; Federica Moscheo performed microbiological analyses; Stefania Giannarelli, Massimo Onor and Stefano Miserocchi performed sediment analyses and revised the paper; Maurizio Azzaro, Antonella Conte, Maria Papale, Marco Graziano and Paul Eric Aspholm participated to the sampling campaigns and helped to write the paper; Luigi Michaud, Angelina Lo Giudice and Maurizio Azzaro designed the research experimentation; Emilio De Domenico revised the paper. All authors read and approved the final manuscript.

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Correspondence to Angelina Lo Giudice.

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Caputo, S., Papale, M., Rizzo, C. et al. Metal Resistance in Bacteria from Contaminated Arctic Sediment is Driven by Metal Local Inputs. Arch Environ Contam Toxicol 77, 291–307 (2019). https://doi.org/10.1007/s00244-019-00628-7

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