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Contribution to interpretation of metal uptake dependence upon the growth phase of microorganisms. The case of uranium (VI) uptake by common yeasts, cultivated at different temperatures, with or without aeration

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Abstract

The dependence of U(VI) uptake on the temperature of cell culture, the air flow during the cultivation process and the age of cells were studied. Saccharomyces cerevisiae, Kluyveromyces marxianus and Debaromyces hansenii were chosen as typical yeasts, which are widely used, in food industries. Our results revealed that the highest metal uptake was obtained from exponential phase cells, which had been cultivated at the optimum temperature of growth, while the air flow during the cultivation process, exhibited no significant effect on the metal uptake. A qualitative interpretation of bibliographic data, concerning the metal uptake on the age of cells is proposed, assuming that qualitative changes in the cell wall structure take place, as the cells pass from exponential to stationary phase, in addition to quantitative modifications, which have been reported in the literature. According to our interpretation, the relative abundances among quantitative and qualitative alterations of cell wall, determine which cells (exponential or stationary) exhibit the higher metal capacity. One type of the suggested qualitative modifications of surface constituent of cell wall, may have been caused by a shortening of a carboxylic acid carbon chain. This type of modification implies, as prerequisite, the decrease of pK a values of cell wall carboxyl groups, with the age of cells. An evidence, supporting our approach, may be the fact that the decrease of pK a values mentioned above, has been observed by other authors.

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References

  1. Landa ER (2003) Mobilization of radionuclides from uranium mill tailings and related waste materials in anaerobic environments. J Radioanal Nucl Chem 255(3):559–563

    Article  CAS  Google Scholar 

  2. Banaszak JE, Rittmann BE, Reed DT (1999) Surface interaction of actinide species and microorganisms: implications for the bioremediation of actinide-organic mixtures. J Radioanal Nucl Chem 241(2):385–435

    Article  CAS  Google Scholar 

  3. Volesky B (2003) Sorption and biosorption. BV. Sorbex, Inc., Montreal, Canada

    Google Scholar 

  4. Kakiuchi H, Amano H, Ichimasa M (2002) Chemical speciation of radionuclides through the microbial process in soils. J Radioanal Nucl Chem 252(2):437–439

    Article  CAS  Google Scholar 

  5. Carro L, Anagnostopoulos V, Lodeiro P, Barriada JL, Herrero R, De Vicente ES (2010) A dynamic proof of mercury elimination from solution through a combined sorption-reduction process. Bioresour Technol. doi:10.1016/j.biortech.2010.06.118

  6. Chakraborty N, Pal R, Ramaswami A, Nayak D, Lahiri S (2006) Diatom: a potential bio-accumulator of gold. J Radioanal Nucl Chem 270(3):645–649

    Article  CAS  Google Scholar 

  7. Nayak D, Lahiri S, Mukhopadhyay A, Pal R (2003) Application of tracer packet technique to the study of the bio-sorption of heavy and toxic metal radionuclides by algae. J Radioanal Nucl Chem 256(3):535–539

    Article  CAS  Google Scholar 

  8. Herrero R, Lodeiro P, Rojo R, Ciorba A, Rodríguez P, Sastre de Vicente ME (2008) The efficiency of the red alga Mastocarpus stellatus for remediation of cadmium pollution. Bioresour Technol 99(10):4138–4146

    Article  CAS  Google Scholar 

  9. Arica MY, Kaçar Y, Genç Ö (2001) Entrapment of white-rot fungus Trametes versicolor in Ca-alginate beads: preparation and biosorption kinetic analysis for cadmium removal from an aqueous solution. Bioresour Technol 80(2):121–129

    Article  CAS  Google Scholar 

  10. Andrès Y, Redercher S, Gerente C, Thouand G (2001) Contribution of biosorption to the behavior of radionuclides in the environment. J Radioanal Nucl Chem 247(1):89–93

    Article  Google Scholar 

  11. Satvatmanesh D, Siavoshi F, Beitollahi MM, Amidi J, Fallahian N (2003) Biosorption of 226Ra in high level natural radiation areas of Ramsar, Iran. J Radioanal Nucl Chem 258(3):483–486

    Article  CAS  Google Scholar 

  12. Vlachou A, Symeopoulos BD, Koutinas AA (2009) A comparative study of neodymium sorption by yeast cells. Radiochim Acta 97(8):437–441

    Article  CAS  Google Scholar 

  13. Sarri S, Misaelides P, Papanikolaou M, Zamboulis D (2009) Uranium removal from acidic aqueous solutions by Saccharomyces cerevisiae, Debaryomyces hansenii, Kluyveromyces marxianus and Candida colliculosa. J Radioanal Nucl Chem 279(3):709–711

    Article  CAS  Google Scholar 

  14. Hafez MB, Fouad A, El-Desouky W (2002) Accumulation of some metal ions on Bacillus licheniformis. J Radioanal Nucl Chem 251(2):249–252

    Article  CAS  Google Scholar 

  15. Yuanyou Y, Ning L, Luo S, Liao J, Jin J, Zhang T, Zhao P (2004) Sorption of 241Am by Aspergillus niger spore and hyphae. J Radioanal Nucl Chem 260(3):659–663

    Article  Google Scholar 

  16. Vasudevan P, Padmavathy V, Dhingra SC (2003) Kinetics of biosorption of cadmium on Baker’s yeast. Bioresour Technol 89:281–287

    Article  CAS  Google Scholar 

  17. Donat R, Aytas S (2005) Adsorption and thermodynamic behavior of uranium(VI) on Ulva sp.-Na bentonite composite adsorbent. J Radioanal Nucl Chem 265(1):107–114

    Article  CAS  Google Scholar 

  18. Das SK, Kedari CS, Shinde SS, Ghosh S, Jambunathan U (2002) Performance of immobilized Saccharomyces cerevisiae in the removal of long lived radionuclides from aqueous nitrate solutions. J Radioanal Nucl Chem 253(2):235–240

    Article  CAS  Google Scholar 

  19. Bai RS, Abraham TE (2002) Studies on enhancement of Cr(VI) biosorption by chemically modified biomass of Rhizopus nigricans. Water Res 36(5):1224–1236

    Article  CAS  Google Scholar 

  20. Daughney CJ, Fowle DA, Fortin D (2001) The effect of growth phase on proton and metal adsorption by Bacillus subtilis. Geochim Cosmochim Acta 65(7):1025–1035

    Article  CAS  Google Scholar 

  21. Russell NJ (2002) Bacterial membranes: the effects of chill storage and food processing. An overview. Int J Food Microbiol 79(1–2):27–34

    Article  CAS  Google Scholar 

  22. Skountzou P, Soupioni M, Bekatorou A, Kanellaki M, Koutinas AA, Marchant R, Banat IM (2003) Lead(II) uptake during Baker’s yeast production by aerobic fermentation of molasses. Process Biochem 38:1479–1482

    Article  CAS  Google Scholar 

  23. Kourkoutas Y, Komaitis M, Koutinas AA, Kanellaki M (2001) Wine production using yeast immobilized on apple pieces at low and room temperatures. J Agric Food Chem 49(3):1417–1425

    Article  CAS  Google Scholar 

  24. Kopsahelis N, Agouridis N, Bekatorou A, Kanellaki M (2007) Comparative study of spent grains and delignified spent grains as yeast supports for alcohol production from molasses. Bioresour Technol 98(7):1440–1447

    Article  CAS  Google Scholar 

  25. Bekatorou A, Psarianos C, Koutinas AA (2006) Production of food grade yeasts. Food Technol Biotechnol 44(3):407–415

    Google Scholar 

  26. Plessas S, Bekatorou A, Gallanagh J, Nigam P, Koutinas AA, Psarianos C (2008) Evolution of aroma volatiles during storage of sourdough breads made by mixed cultures of Kluyveromyces marxianus and Lactobacillus delbrueckii ssp. bulgaricus or Lactobacillus helveticus. Food Chem 107:883–889

    Article  CAS  Google Scholar 

  27. Koutinas AA, Papapostolou H, Dimitrellou D, Kopsahelis N, Katechaki E, Bekatorou A, Bosnea LA (2009) Whey valorization : a complete and novel technology development for dairy industry starter culture production. Bioresour Technol 100:3734–3739

    Article  CAS  Google Scholar 

  28. Marczenko Z (1986) Separation and spectrophotometric determination of elements. Wiley, New York

    Google Scholar 

  29. Beales N (2004) Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Compr Rev Food Sci F 3(1):1–20

    Article  CAS  Google Scholar 

  30. Adams MR, Moss MO (1997) Food microbiology. The Royal Society of Chemistry, Cambridge, England

    Google Scholar 

  31. Russell NJ, Evans RI, ter Steeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28(2):255–261

    Article  CAS  Google Scholar 

  32. Neale EK, Chapman GB (1970) Effect of low temperature on the growth and fine structure of Bacillus subtilis. J Bacteriol 104(1):518–528

    CAS  Google Scholar 

  33. Baleiras Couto MM, Huis-In’t-Veld JHJ (1995) Influence of ethanol and temperature on the cellular fatty acid composition of Zygosaccharomyces bailii spoilage yeasts. J Appl Bacteriol 78(3):327–333

    CAS  Google Scholar 

  34. Norberg AB, Persson H (1984) Accumulation of heavy-metal ions by Zoogloea ramigera. Biotechnol Bioeng 26:239–246

    Article  CAS  Google Scholar 

  35. Shuttleworth KL, Unz RF (1993) Sorption of heavy metals to filamentous bacterium Thiothrix strain A1. Appl Environ Microbiol 59:1274–1282

    CAS  Google Scholar 

  36. Hadi B, Margaritis A, Berruti F, Bergougnou M (2003) Kinetics and equilibrium of cadmium biosorption by yeasts cells S. cerevisiae and K. fragilis. Int J Chem React Eng 3:A47

    Google Scholar 

  37. Macaskie LE, Dean ACR (1984) Cadmium accumulation by a Citrobacter sp. J Gen Microbiol 130:53–62

    CAS  Google Scholar 

  38. Chang J-S, Law R, Chang C-C (1997) Biosorption of lead, copper and cadmium by biomass of Pseudomonas aeruginosa PU21. Water Res 31(7):1651–1658

    Article  CAS  Google Scholar 

  39. Friis N, Meyers-Keith P (1986) Biosorption of uranium and lead by Streptomyces longwoodensis. Biotechnol Bioeng 28:21–28

    Article  CAS  Google Scholar 

  40. Daughney CJ, Fein JB, Yee N (1998) A comparison of the thermodynamics of metal adsorption onto two common bacteria. Chem Geol 144(3–4):161–176

    Article  CAS  Google Scholar 

  41. Hong Y, Brown DG (2006) Cell surface acid-base properties of Escherichia coli and Bacillus brevis and variation as a function of growth phase, nitrogen source and C:N ratio. Colloids Surf B 50(2):112–119

    Article  CAS  Google Scholar 

  42. Mauricio JC, Guijo S, Ortega JM (1991) Relationship between phospholipid and sterol contents in S. cerevisiae and Torulaspora delbrueckii and their fermentation activity in grape musts. Am J Enol Vitic 42(4):301–308

    CAS  Google Scholar 

  43. Berlanga TM, Atanasio C, Mauricio JC, Ortega JM (2001) Influence of aeration on the physiological activity of flor yeasts. J Agric Food Chem 49(7):3378–3384

    Article  CAS  Google Scholar 

  44. Volesky B, May H, Holan ZR (1993) Cadmium biosorption by Saccharomyces cerevisiae. Biotechnol Bioeng 41(8):826–829

    Article  CAS  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge Professor P. Ioannou for his advice and Dr. L. Bosnea for useful discussions.

We thank the European Social Fund (ESF), Operational Program for Educational and Vocational Training II (EPEAEK II), and particularly the Program PYTHAGORAS ΙΙ, for funding the above work.

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Authors and Affiliations

  1. Department of Chemistry, Radiochemistry Lab, University of Patras, 26500, Patras, Greece

    Vasileios A. Anagnostopoulos & Basil D. Symeopoulos

  2. Department of Chemistry, Food Biotechnology Group, University of Patras, 26500, Patras, Greece

    Argyro Bekatorou

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  1. Vasileios A. Anagnostopoulos
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  3. Basil D. Symeopoulos
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Correspondence to Basil D. Symeopoulos.

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Anagnostopoulos, V.A., Bekatorou, A. & Symeopoulos, B.D. Contribution to interpretation of metal uptake dependence upon the growth phase of microorganisms. The case of uranium (VI) uptake by common yeasts, cultivated at different temperatures, with or without aeration. J Radioanal Nucl Chem 287, 665–671 (2011). https://doi.org/10.1007/s10967-010-0811-2

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