Biodegradation

, Volume 19, Issue 1, pp 41–52

Bacterial growth yields on EDTA, NTA, and their biodegradation intermediates

Original Paper

Abstract

Ethylenediaminetetraacetic acid (EDTA) and nitrilotriacetic acid (NTA) are widely used anthropogenic chelating agents for control of metal speciation and are ubiquitous in natural waters and wastewaters. This is the first report of systematic measurement of the growth yields of a mixed culture (BNC1-BNC2) on EDTA and its biodegradation intermediates, and of Aminobacter aminovorans (aka Chelatobacter heintzii) ATCC 29600 on NTA and its biodegradation intermediates. The yields measured for BNC1-BNC2 co-culture were 75.0 g of cell dry weight (CDW) (mole of EDTA)−1, 68.6 g of CDW (mole of ED3 A)−1, 51.2 g of CDW (mole of N,N′-EDDA)−1, 34.5 g of CDW (mole of ED)−1, 26.3 g of CDW (mole of IDA)−1, 12.2 g of CDW (mole of glycine)−1, and 9.7 g of CDW (mole of glyoxylate)−1. The yields measured for A. aminovorans were 44.3 g of CDW (mole of NTA)−1, 37.9 g of CDW (mole of IDA)−1, 15.2 g of CDW (mole of glycine)−1, and 10.4 g of CDW (mole of glyoxylate)−1. The biodegradation pathways of EDTA, NTA, and several of their metabolic intermediates include reactions catalyzed by oxygenase enzymes, which may reduce energy available for cell synthesis. Comparison of measured yields with predicted yields indicates that the effect of oxygenase reaction on cell yield can be quantified experimentally as well as modeled based on thermodynamics.

Keywords

Yield EDTA NTA Intermediate BNC1-BNC2 ATCC 29600 

Abbreviations

EDTA

Ethylenediaminetetraacetic acid

NTA

Nitrilotriacetic acid

ED3A

Ethylenediaminetriacetic acid

3KP

3-ketopiperazine-N,N-diacetate

N,N′-EDDA

N,N′-ethylenediaminediacetic acid

EDMA

Ethylenediaminemonoacetic acid

ED

Ethylenediamine

IDA

Iminodiacetic acid

C. heintzii

Chelatobacter heintzii ATCC 29600

References

  1. Alder AC, Siegrist H, Gujer W, Giger W (1990) Behavior of NTA and EDTA in biological wastewater treatment. Water Res 24:733–742CrossRefGoogle Scholar
  2. Andrews G (1989) Estimating cell and product yield. Bitechnol Bioeng 33:256–265CrossRefGoogle Scholar
  3. Baik MH, Lee KJ (1994) Transport of radioactive solutes in the presence of chelating agents. Ann Nucl Energy 54:81–96CrossRefGoogle Scholar
  4. Bally M, Wilberg E, Kuhni MI, Egli T. (1994) Growth and regulation of enzyme synthesis in the nitrilotriacetic acid (NTA)-degrading bacterium Chelatobacter heintzii ATCC 29600. Microbiology 140:1927–1936CrossRefGoogle Scholar
  5. Barber LB, Brown GK, Kennedy KR, Leenheer JA, Nyes TI, Rostad CE, Thorn KA (1997) Organic constituents that persist during aquifer storage and recovery of reclaimed water in Los Angeles County, California. JAWRA 33:261–272Google Scholar
  6. Barber LB, Brown GK, Zaugg SD (1999) Potential endocrine disrupting organic chemicals in treated municipal wastewater and river water, Upper Midwest, USA. In: Keith L, Jones-Lepp T, Needham L (eds) Analysis of environmental endocrine disruptors, American chemical society symposium series No. 747. American Chemical Society, Washington DC Google Scholar
  7. Bergers P, DeGroot A (1994) The analysis of EDTA in water by HPLC. Water Res 28:639–642CrossRefGoogle Scholar
  8. Bohuslavek J, Payne JW, Liu Y, Bolton HJR, Xun L (2001) Cloning, sequencing, and characterization of a gene cluster involved in EDTA degradation from the bacterium BNC1. Appl Environ Microbiol 67:688–695CrossRefGoogle Scholar
  9. Bolton H Jr, Girvin DC, Plymale AE, Harvey SD, Workman DJ (1996) Degradation of Metal-Nitrilotriacetate (NTA) Complexes by Chelatobacter heintzii. Environ Sci Technol 30:931–938 CrossRefGoogle Scholar
  10. Bucheli-Witschel M, Egli T (2001) Environmental fate and microbial degradation of aminopolycarboxylic acids. FEMS Microbiol Rev 25:69–106CrossRefGoogle Scholar
  11. Cleveland JM, Rees TF (1981) Characterization of plutonium in Maxey Flats radioactive trench leachates. Science 212:1506–1509CrossRefGoogle Scholar
  12. Egli T, Wilennmann H-U, El-Banna T, Auling G (1988) Gram-negative, aerobic, nitrilotriacetate-utilizing bacteria from wastewater and soil. Syst Appl Microbiol 10:297–305Google Scholar
  13. Engelbrecht RS, McKinney RE (1957) Activated sludge cultures developed on pure organic compounds. Sewag Industri Wast 29:1350–1362Google Scholar
  14. Firestone MK, Tiedje JM (1978) Pathway of degradation of nitrilotriacetate by Pseudomonas species. Appl Environ Microbiol 35:955–961Google Scholar
  15. Firestone MK, Tiedje JM (1975) Biodegradation of metal-nitrilotriacetate complexes by a Pseudomonas species: Mechanism of reaction. Appl Microbiol 29:758–764Google Scholar
  16. Frimmel FH, Grenz R, Kordik E, Dietz F (1989) Nitrilotriacetate (NTA) and Ethylenediaminetetraacetate (EDTA) in rivers of the Federal Republic of Germany. Vom Wasser 72:175–184Google Scholar
  17. Frimmel FH (1997) Physiochemical properties of ethylene dinitrilotetraacetic acid and consequences for its distribution in the aquatic environment. In: Schwager MJ (ed) Detergents in the environment. Marcel Dekker, New York, pp 289–312Google Scholar
  18. Gerhardt P, Murray RGE, Wood WA, Krieg NR (1994) Methods for general and molecular bacteriology. American Society for Microbilogy, Washington DCGoogle Scholar
  19. Gschwind N (1992) Biologischer Abbau von EDTA in einem Modellabwasser. Gwf Wasser Abwasser 133:546–549Google Scholar
  20. Henneken L, Nörtemann B, Hempel DC (1995) Influence of physiological conditions on EDTA degradation. Appl Microbiol Biotechnol 44:190–197CrossRefGoogle Scholar
  21. Henneken L, Nörtemann B, Hempel DC (1998) Biological degradation of EDTA: Reaction kinetics and technical approach. J Chem Technol Biotechnol 73:144–152CrossRefGoogle Scholar
  22. Kampfer P, Neef A, Salkinoj-Salonen MS, Busse H-J (2002) Chelatobacter heintzii (Auling et al. 1993) is a later subjective synonym of Aminobacter aminovorans (Urakami et al. 1992). IJSEM 52:835–839Google Scholar
  23. Killey RWD, McHugh JA, Champ DR, Cooper EL, Young JL (1984) Subsurface cobalt-60 migration from a low-level waste disposal site. Environ Sci Technol 18:148–157CrossRefGoogle Scholar
  24. Kluner T (1996) Chemie und Biochemie des mikrobiellen EDTA-Abbaus. Ph.D. thesis. University of Paderborn, Cuvillier Verlag, Gottingen Google Scholar
  25. Kluner T, Hempel DC, Nörtemann B (1998) Metabolism of EDTA and its metal chelates by whole cells and cell-free extracts of strain BNC1. Appl Microbiol Biotechnol 49:194–201CrossRefGoogle Scholar
  26. Liu Y, Louie TM, Payne J, Bohuslavek J, Bolton HJR, Xun L (2001) Identification, purification, and characterization of iminodiacetate oxidase from the EDTA-degrading bacterium BNC1. Appl Environ Microbiol 67:696–701CrossRefGoogle Scholar
  27. Madigan MT, Martinko JM, Parker J (2000) Brock: biology of microorganisms Prentice Hall, New York, p 603Google Scholar
  28. Means JL, Crerar DA, Duguin JO (1978) Migration of radioactive wastes: radionuclide mobilization by complexing agents. Science 200:1477–1481CrossRefGoogle Scholar
  29. McCarty PL (1975) Stoichiometry of biological reactions. Prog Water Tech 7:157–172Google Scholar
  30. Nörtemann B (1992) Total degradation of EDTA by mixed cultures and a bacterial isolate. Appl Environ Microbiol 58:671–676Google Scholar
  31. Nörtemann B (1999) Mini-review: biodegradation of EDTA. Appl Environ Microbiol 51:751–759Google Scholar
  32. Nowack B (2002) Environmental chemistry of aminopolycarboxylate chelating agents. Environ Sci Technol 36:4009–4016CrossRefGoogle Scholar
  33. Parkes DG, Caruso MG, Spradling JEI (1981) Determination of nitrilotriacetic acid in ethylenediaminetetraacetic acid disodium salt by reversed-phase ion pair liquid chromatography. Anal Chem 53:2154–2156CrossRefGoogle Scholar
  34. Payne JW, Bolton HJR, Campbell JA, Xun L (1998) Purification and characterization of EDTA monooxygenase from the EDTA-degrading bacterium BNC1. J Bacteriol 180:3823–3827Google Scholar
  35. Pirt SJ (1975) Principles of microbe and cell cultivation. John Wiley, Sons, New YorkGoogle Scholar
  36. Riley RG, Zachara JM, Wobber FJ (1992) Chemical contaminants on DOE lands and selection of contaminant mixtures for subsurface science research. DOE report: DOE/ER-0547T. Washington, D.C. Google Scholar
  37. Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and application. McCraw-Hill, New YorkGoogle Scholar
  38. Rutgers M, van der Gulden H, van Dam K (1989) Thermodynamic efficiency of bacterial growth calculated from growth yield of pseudomonas oxalaticus OX1 in the chemostat. Biochim Biophys Acta 973:302–307CrossRefGoogle Scholar
  39. Sacher F, Lochow E, Brauch H-J (1998) Synthetic organic complexing agents-analysis and occurrence in surface waters. Vom Wasser 90:31–41Google Scholar
  40. Schmidt CK, Fleig M, Sacher F, Brauch HJ (2004) Occurrence of aminopolycarboxylates in the aquatic environment of Germany. Environ Pollut 131:107–124CrossRefGoogle Scholar
  41. Sillanpaa M (1997) Environmental fate of EDTA and DTPA. Rev Environ Contam Toxicol 152:85–111Google Scholar
  42. Sillanpaa M, Vickackaite V, Niinisto L, Sihvonen. M-L. (1997) Distribution and transportation of ethylenediaminetetraacetic acid and diethylenetriaminepentaacetic acid in lake water and sediment. Chemosphere 35:2797–2805CrossRefGoogle Scholar
  43. Trijbels F, Vogles GD (1966) Degradation of allantoin by Pseudomonas acidovorans. Biochimica et Biophysica Acta 113:292–301Google Scholar
  44. Uetz T, Egli T (1993) Characterization of an inducible, membrane-bound iminodiacetate dehydrogenase from Chelatobacter heintzii ATCC 29600. Biodegradation 3:423–434CrossRefGoogle Scholar
  45. Uetz T, Schneider R, Snozzi M, Egli T (1992) Purification and characterization of a two-component monooxygenase that hydroxylates nitrilotriacetate from “chelatobacter” strain ATCC 296000. J Bacteriol 174:1179–1188Google Scholar
  46. VanBriesen JM (2001) Thermodynamic yield predictions for biodegradation through oxygenase activation reactions. Biodegradation 12(4):265–281CrossRefGoogle Scholar
  47. Weilenmann H-U, Engeli B, Bucheli-Witschel M, Egli T (2004) Isolation and growth characteristics of an EDTA-degrading member of the -subclass of Proteobacteria. Biodegradation 15:289–301CrossRefGoogle Scholar
  48. Wilkinson SG (1970) Cell walls of Pseudomonas species sensitvie to ethylenediaminetetraacetic acid. J Bacteriol 104:1035–1044Google Scholar
  49. Witschel MHU, Weilenmann H-U, Egli T (1995) Degradation of EDTA by a bacterial isolate. Poster presented at the 54 annual meeting of the Swiss Society for Microbiology, LuganoGoogle Scholar
  50. Wolf K, Gilbert PA (1992) EDTA-ethylenediaminetetraacetic acid. In: Hutzinger O (ed) The handbook of environmental chemistry, vol 3. Springer, Berlin, pp 241–259Google Scholar
  51. Woodiwiss CR, Walker RD, Brownridge FA (1979) Concentration of nitrilotriacetate and certain metals in Canadian wastewaters and streams. Water Res 13:599–612CrossRefGoogle Scholar
  52. Xiao J, VanBriesen JM (2005) Expanded thermodynamic model for microbial yield prediction. Biotechol Bioeng 93(1):110–121CrossRefGoogle Scholar
  53. Xu Y, Mortimer MW, Fisher TS, Kahn ML, Brockman FJ, Xun L (1997) Cloning, sequencing, and analysis of a gene cluster from Chelatobacter heintzii ATCC 29600 encoding nitrilotriacetate monooxygenase and NADH:flavin mononucleotide oxidoreductase. J Bacteriol 179:1112–1116Google Scholar
  54. Yuan Z, VanBriesen JM (2002) Yield prediction and stoichiometry of multi-step biodegradation reactions involving oxygenation. Biotechnol Bioeng 80:100–113CrossRefGoogle Scholar
  55. Yuan Z, VanBriesen JM (2005) Analysis of biodegradation intermediates of ethylenediaminetetraacetate (EDTA) and nitrilotriacetate (NTA) by high performance liquid chromatography (HPLC). In: Nowack B, VanBriesen JM (eds) Biogeochemistry of Chelating Agent, American Chemical Society Symposium Series No. 910 American Chemical Society, Washington, D.C, pp 139–148Google Scholar
  56. Yuan Z, VanBriesen JM (2006) The formation of intermediates in EDTA and NTA biodegradation. Env Eng Sci 23(3):533–544CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Civil, Environmental, and Architectural EngineeringUniversity of Colorado at BoulderBoulderUSA
  2. 2.Department of Civil and Environmental EngineeringCarnegie Mellon University, Center for Water Quality in Urban Environmental Systems (Water-QUESt)PittsburghUSA

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