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Volume 152, Issue 9

Anaerobic and aerobic metabolism of glycogen-accumulating organisms selected with propionate as the sole carbon source Free

Abstract

In the microbial competition observed in enhanced biological phosphorus removal (EBPR) systems, an undesirable group of micro-organisms known as glycogen-accumulating organisms (GAOs) compete for carbon in the anaerobic period with the desired polyphosphate-accumulating organisms (PAOs). Some studies have suggested that a propionate carbon source provides PAOs with a competitive advantage over GAOs in EBPR systems; however, the metabolism of GAOs with this carbon source has not been previously investigated. In this study, GAOs were enriched in a laboratory-scale bioreactor with propionate as the sole carbon source, in an effort to better understand their biochemical processes. Based on comprehensive solid-, liquid- and gas-phase chemical analytical data from the bioreactor, a metabolic model was proposed for the metabolism of propionate by GAOs. The model adequately described the anaerobic stoichiometry observed through chemical analysis, and can be a valuable tool for further investigation of the competition between PAOs and GAOs, and for the optimization of the EBPR process. A group of Alphaproteobacteria dominated the biomass (96 % of Bacteria) from this bioreactor, while post-fluorescence hybridization (FISH) chemical staining confirmed that these Alphaproteobacteria produced poly--hydroxyalkanoates (PHAs) anaerobically and utilized them aerobically, demonstrating that they were putative GAOs. Some of the Alphaproteobacteria were related to (16 % of Bacteria), but the specific identity of many could not be determined by FISH. Further investigation into the identity of other GAOs is necessary.

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Keyword(s): acetyl-CoA*, activated acetyl-CoA , EBPR, enhanced biological phosphorus removal , FISH, fluorescence in situ hybridization , GAO, glycogen-accumulating organism , PAO, polyphosphate-accumulating organism , PH2MV, poly-β-hydroxy-2-methylvalerate , PHA, poly-β-hydroxyalkanoate , PHB, poly-β-hydroxybutyrate , PHV, poly-β-hydroxyvalerate , propionyl-CoA*, activated propionyl-CoA , SBR, sequencing batch reactor , TFO, tetrad-forming organism , TOGA, titration and off-gas analysis and VFA, volatile fatty acid
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2006-09-01
2024-04-24
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References

  1. Amann R. I. 1995; In situ identification of microorganisms by whole cell hybridization with rRNA-targeted nucleic acid probes. In Molecular Microbial Ecology Manual pp  1–15 Edited by Akkermans A. D. L., van Elsas J. D., de Bruijn F. J. Dordrecht, Holland: Kluwer Academic Publications;
     [Google Scholar]
  2. Amann R. I, Binder B. J, Olson R. J, Chisholm S. W, Devereux R, Stahl D. A. 1990; Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial-populations. Appl Environ Microbiol 56:1919–1925
     [Google Scholar]
  3. American Public Health Association, American Water Works Association Water Pollution Control Federation (APHA, AWWA & WPCF) 1995 Standard Methods for the Examination of Water and Wastewater, 19th edn. Baltimore: Port City Press;
     [Google Scholar]
  4. Beer M, Seviour E. M, Kong Y, Cunningham M, Blackall L. L, Seviour R. J. 2002; Phylogeny of the filamentous bacterium Eikelboom Type 1851, and design and application of a 16S rRNA targeted oligonucleotide probe for its fluorescence in situ identification in activated sludge. FEMS Microbiol Lett 207:179–183 [CrossRef]
     [Google Scholar]
  5. Beer M, Kong Y. H, Seviour R. J. 2004; Are some putative glycogen accumulating organisms (GAO) in anaerobic : aerobic activated sludge systems members of the alpha-Proteobacteria?. Microbiology 150:2267–2275 [CrossRef]
     [Google Scholar]
  6. Bond P. L, Keller J, Blackall L. L. 1998; Characterisation of enhanced biological phosphorus removal activated sludges with dissimilar phosphorus removal performances. Water Sci Technol 37:567–571 [CrossRef]
     [Google Scholar]
  7. Bouchez T, Patureau D, Dabert P, Wagner M, Delgenes J. P, Moletta R. 2000; Successful and unsuccessful bioaugmentation experiments monitored by fluorescent in situ hybridization. Water Sci Technol 41:61–68
     [Google Scholar]
  8. Chen Y, Randall A. A, McCue T. 2004; The efficiency of enhanced biological phosphorus removal from real wastewater affected by different ratios of acetic to propionic acid. Water Res 38:27–36 [CrossRef]
     [Google Scholar]
  9. Crocetti G. R, Hugenholtz P, Bond P. L, Schuler A, Keller J, Jenkins D, Blackall L. L. 2000; Identification of polyphosphate-accumulating organisms and design of 16S rRNA-directed probes for their detection and quantitation. Appl Environ Microbiol 66:1175–1182 [CrossRef]
     [Google Scholar]
  10. Crocetti G. R, Banfield J. F, Keller J, Bond P. L, Blackall L. L. 2002; Glycogen-accumulating organisms in laboratory-scale and full-scale wastewater treatment processes. Microbiology 148:3353–3364
     [Google Scholar]
  11. Daims H, Bruhl A, Amann R, Schleifer K. H, Wagner M. 1999; The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444 [CrossRef]
     [Google Scholar]
  12. Filipe C. D. M, Daigger G. T, Grady C. P. L. 2001a; A metabolic model for acetate uptake under anaerobic conditions by glycogen accumulating organisms: stoichiometry, kinetics, and the effect of pH. Biotechnol Bioeng 76:17–31 [CrossRef]
     [Google Scholar]
  13. Filipe C. D. M, Daigger G. T, Grady C. P. L. 2001b; Stoichiometry and kinetics of acetate uptake under anaerobic conditions by an enriched culture of phosphorus-accumulating organisms at different pHs. Biotechnol Bioeng 76:32–43 [CrossRef]
     [Google Scholar]
  14. Gottschalk G. 1986 Bacterial Metabolism, 2nd edn. New York: Springer;
     [Google Scholar]
  15. Hesselmann R. P. X, Werlen C, Hahn D, Zehnder A. J. B, van der Meer J. R. 1999; Enrichment, phylogenetic analysis and detection of a bacterium that performs enhanced biological phosphate removal in activated sludge. Syst Appl Microbiol 22:454–465 [CrossRef]
     [Google Scholar]
  16. Kong Y. H, Ong S. L, Ng W. J, Liu W. T. 2002; Diversity and distribution of a deeply branched novel proteobacterial group found in anaerobic–aerobic activated sludge processes. Environ Microbiol 4:753–757 [CrossRef]
     [Google Scholar]
  17. Levantesi C, Serafim L. S, Crocetti G. R, Lemos P. C, Rossetti S, Blackall L. L, Reis M. A. M, Tandoi V. 2002; Analysis of the microbial community structure and function of a laboratory scale enhanced biological phosphorus removal reactor. Environ Microbiol 4:559–569 [CrossRef]
     [Google Scholar]
  18. Liu W. T, Nielsen A. T, Wu J. H, Tsai C. S, Matsuo Y, Molin S. 2001; In situ identification of polyphosphate- and polyhydroxyalkanoate-accumulating traits for microbial populations in a biological phosphorus removal process. Environ Microbiol 3:110–122 [CrossRef]
     [Google Scholar]
  19. Manz W, Amann R, Ludwig W, Wagner M, Schleifer K. H. 1992; Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria – problems and solutions. Syst Appl Microbiol 15:593–600 [CrossRef]
     [Google Scholar]
  20. Meyer R. L, Saunders A. M, Blackall L. L. 2006; Putative glycogen-accumulating organisms belonging to Alphaproteobacteria identified through rRNA-based stable isotope probing. Microbiology 152:419–429 [CrossRef]
     [Google Scholar]
  21. Neef A. 1997 Anwendung der in situ Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen PhD thesis Technische Universität München;
     [Google Scholar]
  22. Nielsen A. T, Liu W. T, Filipe C, Grady L, Molin S, Stahl D. A. 1999; Identification of a novel group of bacteria in sludge from a deteriorated biological phosphorus removal reactor. Appl Environ Microbiol 65:1251–1258
     [Google Scholar]
  23. Oehmen A, Yuan Z, Blackall L. L, Keller J. 2004; Short-term effects of carbon source on the competition of polyphosphate accumulating organisms and glycogen accumulating organisms. Water Sci Technol 50:139–144
     [Google Scholar]
  24. Oehmen A, Yuan Z. G, Blackall L. L, Keller J. 2005a; Comparison of acetate and propionate uptake by polyphosphate accumulating organisms and glycogen accumulating organisms. Biotechnol Bioeng 91:162–168 [CrossRef]
     [Google Scholar]
  25. Oehmen A, Zeng R. J, Yuan Z. G, Keller J. 2005b; Anaerobic metabolism of propionate by polyphosphate-accumulating organisms in enhanced biological phosphorus removal systems. Biotechnol Bioeng 91:43–53 [CrossRef]
     [Google Scholar]
  26. Oehmen A, Saunders A. M, Vives M. T, Yuan Z, Keller J. 2006; Competition between polyphosphate and glycogen accumulating organisms in enhanced biological phosphorus removal systems with acetate and propionate as carbon sources. J Biotechnol 123:22–32 [CrossRef]
     [Google Scholar]
  27. Onda S, Hiraishi A, Matsuo Y, Takii S. 2002; Polyphasic approaches to the identification of predominant polyphosphate-accumulating organisms in a laboratory-scale anaerobic/aerobic activated sludge system. J Gen Appl Microbiol 48:43–54 [CrossRef]
     [Google Scholar]
  28. Ostle A. G, Holt J. G. 1982; Nile blue A as a fluorescent stain for poly-beta-hydroxybutyrate. Appl Environ Microbiol 44:238–241
     [Google Scholar]
  29. Pijuan M, Saunders A. M, Guisasola A, Baeza J. A, Casas C, Blackall L. L. 2004; Enhanced biological phosphorus removal in a sequencing batch reactor using propionate as the sole carbon source. Biotechnol Bioeng 85:56–67 [CrossRef]
     [Google Scholar]
  30. Pratt S, Yuan Z, Gapes D, Dorigo M, Zeng R. J, Keller J. 2003; Development of a novel titration and off-gas analysis (TOGA) sensor for study of biological processes in wastewater treatment systems. Biotechnol Bioeng 81:482–495 [CrossRef]
     [Google Scholar]
  31. Satoh H, Mino T, Matsuo T. 1994; Deterioration of enhanced biological phosphorus removal by the domination of microorganisms without polyphosphate accumulation. Water Sci Technol 30:203–211
     [Google Scholar]
  32. Saunders A. M, Oehmen A, Blackall L. L, Yuan Z, Keller J. 2003; The effect of GAOs (glycogen accumulating organisms) on anaerobic carbon requirements in full-scale Australian EBPR (enhanced biological phosphorus removal) plants. Water Sci Technol 47:37–43
     [Google Scholar]
  33. Seviour R. J, Mino T, Onuki M. 2003; The microbiology of biological phosphorus removal in activated sludge systems. FEMS Microbiol Rev 27:99–127 [CrossRef]
     [Google Scholar]
  34. Smolders G. J. F, Vandermeij J, Vanloosdrecht M. C. M, Heijnen J. J. 1994a; Stoichiometric model of the aerobic metabolism of the biological phosphorus removal process. Biotechnol Bioeng 44:837–848 [CrossRef]
     [Google Scholar]
  35. Smolders G. J. F, Vandermeij J, Vanloosdrecht M. C. M, Heijnen J. J. 1994b; Model of the anaerobic metabolism of the biological phosphorus removal process – stoichiometry and pH influence. Biotechnol Bioeng 43:461–470 [CrossRef]
     [Google Scholar]
  36. Smolders G. J. F, Vandermeij J, Vanloosdrecht M. C. M, Heijnen J. J. 1995; A structured metabolic model for anaerobic and aerobic stoichiometry and kinetics of the biological phosphorus removal process. Biotechnol Bioeng 47:277–287 [CrossRef]
     [Google Scholar]
  37. Thomas M, Wright P, Blackall L, Urbain V, Keller J. 2003; Optimisation of Noosa BNR plant to improve performance and reduce operating costs. Water Sci Technol 47:141–148
     [Google Scholar]
  38. Voet D, Voet J. G. 1990 Biochemistry New York: Wiley;
     [Google Scholar]
  39. Whang L. M, Park J. K. 2002; Competition between polyphosphate- and glycogen-accumulating organisms in biological phosphorus removal systems – effect of temperature. Water Sci Technol 46:191–194
     [Google Scholar]
  40. Wong M. T, Tan F. M, Ng W. J, Liu W. T. 2004; Identification and occurrence of tetrad-forming Alphaproteobacteria in anaerobic–aerobic activated sludge processes. Microbiology 150:3741–3748 [CrossRef]
     [Google Scholar]
  41. Zeng R, Yuan Z, Keller J, van Loosdrecht M. C. M. 2002; Proposed modifications to metabolic model for glycogen-accumulating organisms under anaerobic conditions. Biotechnol Bioeng 80:277–279 [CrossRef]
     [Google Scholar]
  42. Zeng R. J, Saunders A. M, Yuan Z, Blackall L. L, Keller J. 2003a; Identification and comparison of aerobic and denitrifying polyphosphate-accumulating organisms. Biotechnol Bioeng 83:140–148 [CrossRef]
     [Google Scholar]
  43. Zeng R. J, Yuan Z. G, Keller J, van Loosdrecht M. C. M. 2003b; Metabolic model for glycogen-accumulating organisms in anaerobic/aerobic activated sludge systems. Biotechnol Bioeng 81:92–105 [CrossRef]
     [Google Scholar]
  44. Zilles J. L, Peccia J, Noguera D. R. 2002; Microbiology of enhanced biological phosphorus removal in aerated-anoxic orbal processes. Water Environ Res 74:428–436 [CrossRef]
     [Google Scholar]
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Anaerobic and aerobic metabolism of glycogen-accumulating organisms selected with propionate as the sole carbon source
Microbiology 152, 2767 (2006); https://doi.org/10.1099/mic.0.28065-0
/content/journal/micro/10.1099/mic.0.28065-0
/content/journal/micro/10.1099/mic.0.28065-0
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