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Mixed-Species Biofilms Cultured from an Oil Sand Tailings Pond can Biomineralize Metals

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Abstract

Here, we used an in vitro biofilm approach to study metal resistance and/or tolerance of mixed-species biofilms grown from an oil sand tailings pond in northern Alberta, Canada. Metals can be inhibitory to microbial hydrocarbon degradation. If microorganisms are exposed to metal concentrations above their resistance levels, metabolic activities and hydrocarbon degradation can be slowed significantly, if not inhibited completely. For this reason, bioremediation strategies may be most effective if metal-resistant microorganisms are used. Viability was measured after exposure to a range of concentrations of ions of Cu, Ag, Pb, Ni, Zn, V, Cr, and Sr. Mixed-species biofilms were found to be extremely metal resistant; up to 20 mg/L of Pb, 16 mg/L of Zn, 1,000 mg/L of Sr, and 3.2 mg/L of Ni. Metal mineralization was observed by visualization with scanning electron microscopy with metal crystals of Cu, Ag, Pb, and Sr exuding from the biofilms. Following metal exposure, the mixed-species biofilms were analyzed by molecular methods and were found to maintain high levels of species complexity. A single species isolated from the community (Rhodococcus erythropolis) was used as a comparison against the mixed-community biofilm and was seen to be much less tolerant to metal stress than the community and did not biomineralize the metals.

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References

  1. Abou-Shanab RAI, van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367

    Article  CAS  PubMed  Google Scholar 

  2. Amor L, Kennes C, Veiga MC (2001) Kinetics of inhibition in the biodegradation of monoaromatic hydrocarbons in presence of heavy metals. Bioresour Technol 78:181–185

    Article  CAS  PubMed  Google Scholar 

  3. Arrete M, Heap JM, Christofi N (1997) The effect of toxic discharges on ATP content in activated sludge. Environ Toxicol Water Qual 12:23–29

    Article  Google Scholar 

  4. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Fedorak PM, Coy DL, Salloum MJ, Dudas MJ (2002) Methanogenic potential of tailings samples from oil sands extraction plants. Can J Microbiol 48:21–33

    Article  CAS  PubMed  Google Scholar 

  6. Ferguson W, Braunschweiger KI, Braunschweiger WR, Smith JR, McCormick JJ, Wasmann CC, Jarvis NP, Bell DH, Good NE (1980) Hydrogen ion buffers for biological research. Anal Biochem 104:300–310

    Article  CAS  PubMed  Google Scholar 

  7. Giller KE, Witter E, McGrath SP (2009) Heavy metals and soil microbes. Soil Biol Biochem 41:2031–2037

    Article  CAS  Google Scholar 

  8. Golby S, Ceri H, Gieg LM, Chatterjee I, Marques LLR, Turner RJ (2012) Evaluation of microbial biofilm communities from an Alberta oil sands tailings pond. FEMS Microbiol Ecol 79:240–250

    Article  CAS  PubMed  Google Scholar 

  9. Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467

    Article  CAS  PubMed  Google Scholar 

  10. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  PubMed  Google Scholar 

  11. Harrison JJ, Turner RJ, Ceri H (2005) High-throughput metal susceptibility testing of microbial biofilms. BMC Microbiol 5:53

    Article  PubMed Central  PubMed  Google Scholar 

  12. Harrison JJ, Ceri H, Stremick CA, Turner RJ (2004) Biofilm susceptibility to metal toxicity. Environ Microbiol 6:1220–1227

    Article  CAS  PubMed  Google Scholar 

  13. Harrison JJ, Ceri H, Turner RJ (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5:928–938

    Article  CAS  PubMed  Google Scholar 

  14. Harrison JJ, Ceri H, Yerly J, Stremick CA, Hu Y, Martinuzzi R, Turner RJ (2006) The use of microscopy and three-dimensional visualization to evaluate the structure of microbial biofilms cultivated in the Calgary Biofilm Device. Biol Proced Online 8:94–215

    Article  Google Scholar 

  15. Harrison JJ, Stremick CA, Turner RJ, Allan ND, Olson ME, Ceri H (2010) Microtiter susceptibility testing of microbes growing on peg lids: a miniaturized biofilm model for high-throughput screening. Nat Protoc 5:1236–1254

    Article  CAS  PubMed  Google Scholar 

  16. Herman DC, Fedorak PM, Costerton JW (1993) Biodegradation of cycloalkane carboxylic acids in oil sand tailings. Can J Microbiol 39:576–580

    Article  CAS  PubMed  Google Scholar 

  17. Herman DC, Fedorak PM, MacKinnon MD, Costerton JW (1994) Biodegradation of naphthenic acids by microbial populations indigenous to oil sands tailings. Can J Microbiol 40:467–477

    Article  CAS  PubMed  Google Scholar 

  18. Holowenko FM, MacKinnon MD, Fedorak PM (2000) Methanogens and sulfate-reducing bacteria in oil sands fine tailings waste. Can J Microbiol 46:927–937

    Article  CAS  PubMed  Google Scholar 

  19. Hughes MN, Poole RK (1991) Metal speciation and microbial growth the hard and soft facts. J Gen Microbiol 137:725–734

    Article  CAS  Google Scholar 

  20. Lemire J, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11:371–384

    Article  CAS  PubMed  Google Scholar 

  21. Malik A (2004) Metal bioremediation through growing cells. Environ Intern 30:261–278

    Article  CAS  Google Scholar 

  22. Nies DH, Silver S (2007) Moleuclar microbiology of heavy metals. Microbiol Monogr 6

  23. Nix PG, Martin RW (1992) Detoxification and reclamation of suncor’s oil sand tailings ponds. Environ Toxicol Water Qual 7:171–188

    Article  CAS  Google Scholar 

  24. Penner TJ, Foght JM (2010) Mature fine tailings from oil sands processing harbour diverse methanogenic communities. Can J Microbiol 56:459–470

    Article  CAS  PubMed  Google Scholar 

  25. Pradhan AA, Levine AD (1995) Microbial biosorption of copper and lead from aqueous systems. Sci Total Environ 170:209–220

    Article  CAS  PubMed  Google Scholar 

  26. Ramos-Padron E, Bordenave S, Lin S, Bhaskar IM, Dong X, Sensen CW, Fournier J, Voordouw G, Gieg LM (2011) Carbon and sulfur cycling by microbial communities in a gypsum-treated oil sands tailings pond. Environ Sci Technol 45:439–446

    Article  CAS  PubMed  Google Scholar 

  27. Rosche B, Li XZ, Hauer B, Schmid A, Buehler K (2009) Microbial biofilms: a concept for industrial catalysis? Trends Biotechnol 27:636–643

    Article  CAS  PubMed  Google Scholar 

  28. Ryan RP, Ryan DJ, Dowling DN (2005) Multiple metal resistant transferable phenotypes in bacteria as indicators of soil contamination with heavy metals. J Soils Sediments 5:95–100

    Article  CAS  Google Scholar 

  29. Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093–1101

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Santopolo LL, Marchi EE, Frediani LL, Decorosi FF, Viti CC, Giovannetti LL (2012) A novel approach combining the calgary biofilm device and phenotype microarray for the characterization of the chemical sensitivity of bacterial biofilms. Biofouling 28:1023–1032

    Article  CAS  PubMed  Google Scholar 

  31. Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397

    Article  CAS  PubMed  Google Scholar 

  32. Turgay OC, Bilen S (2012) The role of plant growth-promoting rhixosphere bacteria in toxic metal extraction by Brassica spp. in the plant family Brassicaceae contribution towards phytoremediation. (Anjum NA et al editors). Springer. Environ Pollut 21:213–238

    Article  CAS  Google Scholar 

  33. Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. App Environ Microbiol 69:2313–2320

    Article  CAS  Google Scholar 

  34. Workentine ML, Harrison JJ, Stenroos PU, Ceri H, Turner RJ (2008) Pseudomonas fluorescens view of the periodic table. Environ Microbiol 10:238–250

    CAS  PubMed  Google Scholar 

  35. Wyndham RC, Costerton JW (1981) Heterotrophic potentials and hydrocarbon biodegradation potentials of sediment microorganisms within the Athabasca oil sands deposit. App Environ Microbiol 41:783–790

    CAS  Google Scholar 

  36. Xia L, Yin C, Cai L, Qiu G, Qin W, Peng B, Liu J (2010) Metabolic changes of Acidithiobacillus caldus under Cu2+ stress. J Basic Microbiol 50:591–598

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank members of the Petroleum Microbiology Research Group (Drs. Gerrit Voordouw and Lisa Gieg) of which is supported by Genome Canada, Genome Alberta, the Government of Alberta, and Genome BC. An oil sand operator from the Athabasca region is gratefully acknowledged for supplying the tailings pond sample. The research was supported by an NSERC Strategic grant to RJT and HC.

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Correspondence to Raymond J. Turner.

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ESM 1

Table summarizing the organisms identified through 16S rRNA gene 454 pyrosequencing under the different metal stresses. The SEM figures of Zn, Ni, Cr, and V exposed biofilms, which did not display metal crystals. SEM figures of blank CBD pegs exposed to the metals. (PDF 2.37 MB)

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Golby, S., Ceri, H., Marques, L.L.R. et al. Mixed-Species Biofilms Cultured from an Oil Sand Tailings Pond can Biomineralize Metals. Microb Ecol 68, 70–80 (2014). https://doi.org/10.1007/s00248-013-0331-z

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  • DOI: https://doi.org/10.1007/s00248-013-0331-z

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