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

  • Simona Caputo
  • Maria Papale
  • Carmen Rizzo
  • Stefania Giannarelli
  • Antonella Conte
  • Federica Moscheo
  • Marco Graziano
  • Paul Eric Aspholm
  • Massimo Onor
  • Emilio De Domenico
  • Stefano Miserocchi
  • Luigi Michaud
  • Maurizio Azzaro
  • Angelina Lo GiudiceEmail author
Article

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.

Notes

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.

Author Contributions

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.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

244_2019_628_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 11 kb)
244_2019_628_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 13 kb)

References

  1. Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98:2243–2257CrossRefGoogle 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 12:44CrossRefGoogle 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 31:261–273Google 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 12:193CrossRefGoogle 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 25:3389–3402CrossRefGoogle Scholar
  6. AMAP (2002) AMAP assessment: heavy metals in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), OsloGoogle Scholar
  7. AMAP (2011) AMAP assessment 2011: mercury in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, NorwayGoogle Scholar
  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 201:211–214CrossRefGoogle Scholar
  9. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207CrossRefGoogle Scholar
  10. Ceylan O, Ugur A (2012) Bio-monitoring of heavy metal resistance in Pseudomonas and Pseudomonas related genus. J Biol Environ Sci 6:233–242Google 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 9:38–43Google Scholar
  12. Dauvalter V, Rognerud S (2001) Heavy metals pollution in sediments of the Pasvik River drainage. Chemosphere 42:9–18CrossRefGoogle 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 45:171–185CrossRefGoogle 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 41:151–156CrossRefGoogle 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 28:261–268CrossRefGoogle Scholar
  16. Habi S, Daba H (2009) Plasmid incidence, antibiotic and metal resistance among enterobacteriaceae isolated from Algeria stream. Pak J Appl Sci 12:1474–1482Google 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 25:1089–1102CrossRefGoogle 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 22:240–250CrossRefGoogle Scholar
  19. Malik A, Khan IF, Aleem A (2002) Plasmid incidence in bacteria from agricultural and industrial soils. World J Microbiol Biotechnol 18:827–833CrossRefGoogle 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 37:227–235CrossRefGoogle 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 230:63–71CrossRefGoogle 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 61:429–435CrossRefGoogle Scholar
  23. Nies DH (1999) Microbial heavy metals resistances. Appl Microbiol Biotechnol 51:730–750CrossRefGoogle Scholar
  24. Nies DH (2000) Heavy metal resistant bacteria as extremophiles: molecular physiology and biotechnological use of Ralstonia sp. CH34. Extremophiles 4:77–82CrossRefGoogle 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 14:10197–10228CrossRefGoogle 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 6:893–903CrossRefGoogle 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 168:155–168CrossRefGoogle Scholar
  28. Raja ECA, Selvam GS (2006) Isolation and characterization of a metalresistant Pseudomonas aeruginosa strain. World J Microbiol Biotechnol 22:577–586CrossRefGoogle 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 53:1185–1189Google 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 83:435–445CrossRefGoogle Scholar
  31. Sumampouw OJ, Risjani Y (2014) Bacteria as indicators of environmental pollution: review. Int J Ecosyst 4:251–258Google Scholar
  32. Tada Y, Inoue T (2000) Use of oligotrophic bacteria for the biological monitoring of heavy metals. J Appl Microbiol 88:154–160CrossRefGoogle 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 22:4673–4680CrossRefGoogle 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 35:593–607CrossRefGoogle 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 8:348–357CrossRefGoogle Scholar
  36. Vaz-Moreira I, Nunes OC, Manaia CM (2011) Diversity and antibiotic resistance patterns of Sphingomonadaceae isolates from drinking water. Appl Environ Microbiol 77:5697–5706CrossRefGoogle Scholar
  37. Zakaria ZA, Jaapar J, Ahmad WA (2004) Bacteria as bioindicators for metal contamination. In :Biomonitoring in tropical coastal ecosystems, Phang and Brown, 131–135Google Scholar
  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 72:582–594CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Simona Caputo
    • 1
  • Maria Papale
    • 1
  • Carmen Rizzo
    • 1
  • Stefania Giannarelli
    • 2
  • Antonella Conte
    • 1
  • Federica Moscheo
    • 1
  • Marco Graziano
    • 1
  • Paul Eric Aspholm
    • 3
  • Massimo Onor
    • 4
  • Emilio De Domenico
    • 1
  • Stefano Miserocchi
    • 5
  • Luigi Michaud
    • 1
  • Maurizio Azzaro
    • 6
  • Angelina Lo Giudice
    • 1
    • 6
    Email author
  1. 1.Department of Chemical, Biological, Pharmaceutical and Environmental SciencesUniversity of MessinaMessinaItaly
  2. 2.Department of Chemistry and Industrial ChemistryUniversity of PisaPisaItaly
  3. 3.Norwegian Institute of Bioeconomy Research (NIBIO)SvanvikNorway
  4. 4.Institute of Chemistry of Organometallic CompoundsNational Research Council (ICCOM-CNR)PisaItaly
  5. 5.Institute of Marine SciencesNational Research Council (ISMAR-CNR)BolognaItaly
  6. 6.Institute of Marine Biological Resources and BiotechnologyNational Research Council (IRBIM-CNR)MessinaItaly

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