The effect of free nitrous acid on the anabolic and catabolic processes of glycogen accumulating organisms

Ye, Liu, Pijuan, Maite and Yuan, Zhiguo (2010) The effect of free nitrous acid on the anabolic and catabolic processes of glycogen accumulating organisms. Water Research, 44 9: 2901-2909. doi:10.1016/j.watres.2010.02.010


Author Ye, Liu
Pijuan, Maite
Yuan, Zhiguo
Title The effect of free nitrous acid on the anabolic and catabolic processes of glycogen accumulating organisms
Journal name Water Research   Check publisher's open access policy
ISSN 0043-1354
1879-2448
Publication date 2010-05
Year available 2010
Sub-type Article (original research)
DOI 10.1016/j.watres.2010.02.010
Volume 44
Issue 9
Start page 2901
End page 2909
Total pages 9
Editor David Dixon
Jean-Claude Block
Mogens Henze
Place of publication Oxford, United Kingdom
Publisher Pergamon Press
Collection year 2011
Language eng
Abstract Nitrite/Free Nitrous Acid (FNA) has previously been shown to inhibit aerobic and anoxic phosphate uptake by polyphosphate accumulating organisms (PAOs). The inhibitory effect of FNA on the aerobic metabolism of Glycogen Accumulating Organisms (GAOs) is investigated. A culture highly enriched (92 ± 3%) in Candidatus Competibacter phosphatis (hereafter called Competibacter) was used. The experimental data strongly suggest that FNA likely directly inhibits the growth of Competibacter, with 50% inhibition occurring at 1.5 × 10−3 mgN-HNO2/L (equivalent to approximately 6.3 mgN-NO2−/L at pH 7.0). The inhibition is well described by an exponential function. The organisms ceased to grow at an FNA concentration of 7.1 × 10−3 mgN-HNO2/L. At this FNA level, glycogen production, another anabolic process performed by GAOs in parallel to growth, decreased by 40%, while the consumption of polyhydroxyalkanoates (PHAs), the intracellular carbon and energy sources for GAOs, decreased by approximately 50%. FNA likely inhibited either or both of the PHA oxidation and glycogen production processes, but to a much less extent in comparison to the inhibition on growth. The comparison of these results with those previously reported on PAOs suggest that FNA has much stronger inhibitory effects on the aerobic metabolism of PAOs than on GAOs, and may thus provide a competitive advantage to GAOs over PAOs in enhanced biological phosphorus removal (EBPR) systems.
Keyword Enhanced biological phosphorus removal
Aerobic metabolism
Nitrite
Free nitrous acid
Inhibition
Glycogen accumulating organisms
References Almeida et al., 1995 J.S. Almeida, S.M. Julio, M.A.M. Reis and M.J.T. Carrondo, Nitrite inhibition of denitrification by Pseudomonas fluorescens, Biotechnology and Bioengineering 46 (3) (1995), pp. 194–201. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (57) Amann, 1995 R.I. Amann, Fluorescently labeled, ribosomal-RNA-targeted oligonucleotide probes in the study of microbial ecology, Molecular Ecology 4 (5) (1995), pp. 543–553. Anthonisen et al., 1976 A.C. Anthonisen, R.C. Loehr, T.B.S. Prakasam and E.G. Srinath, Inhibition of nitrification by ammonia and nitrous-acid, Journal Water Pollution Control Federation 48 (5) (1976), pp. 835–852. View Record in Scopus | Cited By in Scopus (527) APHA, 1995 APHA, Standard Methods for the Examination of Water and Wastewater (19th ed.), American Public Health Association, Washington, DC (1995). Crocetti et al., 2000 G.R. Crocetti, P. Hugenholtz, P.L. Bond, A. Schuler, J. Keller, D. Jenkins and L.L. Blackall, Identification of polyphosphate-accumulating organisms and design of 16s rRNA-directed probes for their detection and quantitation, Applied and Environmental Microbiology 66 (3) (2000), pp. 1175–1182. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (258) Crocetti et al., 2002 G.R. Crocetti, J.F. Banfield, J. Keller, P.L. Bond and L.L. Blackall, Glycogen accumulating organisms in laboratory-scale and full-scale wastewater treatment processes, Microbiology 148 (11) (2002), pp. 3353–3364. Dai et al., 2007 Y. Dai, Z. Yuan, K. Jack and J. Keller, Production of targeted poly(3-hydroxyalkanoates) copolymers by glycogen accumulating organisms using acetate as sole carbon source, Journal of Biotechnology 129 (3) (2007), pp. 489–497. Article | PDF (722 K) | View Record in Scopus | Cited By in Scopus (21) Daims et al., 1999 H. Daims, A. Bruhl, R. Amann, K.H. Schleifer and M. Wagner, The domain-specific probe EUB338 is insufficient for the detection of all bacteria: Development and evaluation of a more comprehensive probe set, Systematic and Applied Microbiology 22 (3) (1999), pp. 434–444. View Record in Scopus | Cited By in Scopus (698) Dawes and Ribbons, 1964 E.A. Dawes and D.W. Ribbons, Some aspects of the endogenous metabolism of bacteria, Bacteriological Reviews 28 (2) (1964), pp. 126–140. Filipe et al., 2001a C.D.M. Filipe, G.T. Daigger and C.P.L. Grady, A metabolic model for acetate uptake under anaerobic conditions by glycogen accumulating organisms: Stoichiometry, kinetics, and the effect of ph, Biotechnology and Bioengineering 76 (1) (2001), pp. 17–31. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (87) Filipe et al., 2001b C.D.M. Filipe, G.T. Daigger and C.P.L. Grady, Effects of pH on the rates of aerobic metabolism of phosphate-accumulating and glycogen-accumulating organisms, Water Environment Research 73 (2) (2001), pp. 213–222. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (41) Fux et al., 2003 C. Fux, K. Lange, A. Faessler, P. Huber, B. Grueniger and H. Siegrist, Nitrogen removal from digester supernatant via nitrite - SBR or SHARON?, Water Science and Technology 48 (8) (2003), pp. 9–18. View Record in Scopus | Cited By in Scopus (39) Hu et al., 2003 J.Y. Hu, S.L. Ong, W.J. Ng, F. Lu and X.J. Fan, A new method for characterizing denitrifying phosphorus removal bacteria by using three different types of electron acceptors, Water Research 37 (14) (2003), pp. 3463–3471. Article | PDF (135 K) | View Record in Scopus | Cited By in Scopus (49) Lemaire et al., 2008 R. Lemaire, M. Marcelino and Z. Yuan, Achieving the nitrite pathway using aeration phase length control and step-feed in an SBR removing nutrients from abattoir wastewater, Biotechnology and Bioengineering 100 (6) (2008), pp. 1228–1236. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (13) Liu et al., 1994 W.T. Liu, T. Mino, K. Nakamura and T. Matsuo, Role of glycogen in acetate uptake and polyhydroxyalkanoate synthesis in anaerobic-aerobic activated-sludge with a minimized polyphosphate content, Journal of Fermentation and Bioengineering 77 (5) (1994), pp. 535–540. Abstract | PDF (700 K) | View Record in Scopus | Cited By in Scopus (84) van Loosdrecht et al., 2009 M.C.M. van Loosdrecht, A. Oehmen, C.M. Hooijmans, D. Brdjanovic, H.J. Gijzen, Z. Yuan and C.M. Lopez-Vazquez, Response to the comment on “Modelling the PAO-GAO competition: Effects of carbon source, pH and Temperature” by Dwight Houweling et al, Water Research 43 (11) (2009), pp. 2950–2951. Article | PDF (130 K) | View Record in Scopus | Cited By in Scopus (1) Ma et al., 2009 Y. Ma, Y. Peng, S. Wang, Z. Yuan and X. Wang, Achieving nitrogen removal via nitrite in a pilot-scale continuous pre-denitrification plant, Water Research 43 (3) (2009), pp. 563–572. Article | PDF (462 K) | View Record in Scopus | Cited By in Scopus (7) Meinhold et al., 1999 J. Meinhold, E. Arnold and S. Isaacs, Effect of nitrite on anoxic phosphate uptake in biological phosphorus removal activated sludge, Water Research 33 (8) (1999), pp. 1871–1883. Article | PDF (614 K) | View Record in Scopus | Cited By in Scopus (59) Metcalf and Eddy, 1991 Metcalf and Eddy, Wastewater Engineering: Treatment, Disposal and Reuse, McGraw-Hill Companies, Singapore (1991). Murnleitner et al., 1997 E. Murnleitner, T. Kuba, M.C.M. van Loosdrecht and J.J. Heijnen, An integrated metabolic model for the aerobic and denitrifying biological phosphorus removal, Biotechnology and Bioengineering 54 (5) (1997), pp. 434–450. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (105) Oehmen et al., 2005 A. Oehmen, B. Keller-Lehmann, R.J. Zeng, Z. Yuan and E. Keller, Optimisation of poly-beta-hydroxyalkanoate analysis using gas chromatography for enhanced biological phosphorus removal systems, Journal of Chromatography A 1070 (1–2) (2005), pp. 131–136. Article | PDF (165 K) | View Record in Scopus | Cited By in Scopus (38) Oehmen et al., 2006 A. Oehmen, R.J. Zeng, A.M. Saunders, L.L. Blackall, J. Keller and Z. Yuan, Anaerobic and aerobic metabolism of glycogen-accumulating organisms selected with propionate as the sole carbon source, Microbiology 152 (9) (2006), pp. 2767–2778. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (24) Oehmen et al., 2007 A. Oehmen, P.C. Lemos, G. Carvalho, Z. Yuan, J. Keller, L.L. Blackall and M.A.M. Reis, Advances in enhanced biological phosphorus removal: from micro to macro scale, Water Research 41 (11) (2007), pp. 2271–2300. Article | PDF (808 K) | View Record in Scopus | Cited By in Scopus (71) Oleary and Solberg, 1976 V. Oleary and M. Solberg, Effect of sodium nitrite inhibition on intracellular thiol-groups and on activity of certain glycolytic enzymes in Clostridium perfringens, Applied and Environmental Microbiology 31 (2) (1976), pp. 208–212. View Record in Scopus | Cited By in Scopus (11) Reddy et al., 1983 D. Reddy, J.R. Lancaster and D.P. Cornforth, Nitrite inhibition of Clostridium botulinum: electron spin resonance detection of iron nitric-oxide complexes, Science 221 (4612) (1983), pp. 769–770. View Record in Scopus | Cited By in Scopus (59) Rowe et al., 1979 J.J. Rowe, J.M. Yarbrough, J.B. Rake and R.G. Eagon, Nitrite inhibition of aerobic-bacteria, Current Microbiology 2 (1) (1979), pp. 51–54. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (11) Saito et al., 2004 T. Saito, D. Brdjanovic and M.C.M. van Loosdrecht, Effect of nitrite on phosphate uptake by phosphate accumulating organisms, Water Research 38 (17) (2004), pp. 3760–3768. Article | PDF (321 K) | View Record in Scopus | Cited By in Scopus (41) Saito et al., 2007 T. Saito, K. Takahashi, Y. Yoshida and K. Tanaka, Unstable nitrtie inhibition of phosphate uptake caused by aerobic nitrite denitrification of phosphate-accumulating organisms, Proceedings of the Nutrient Removal Conference- The State of the Art. 4–7 March, Baltimore, Maryland, USA (2007). Saunders et al., 2003 A.M. Saunders, A. Oehmen, L.L. Blackall, Z. Yuan and J. Keller, The effect of GAOs (glycogen accumulating organisms) on anaerobic carbon requirements in full-scale Australian EBPR (enhanced biological phosphorus removal) plants, Water Science and Technology 47 (11) (2003), pp. 37–43. View Record in Scopus | Cited By in Scopus (45) Sin et al., 2008 G. Sin, K. Niville, G. Bachis, T. Jiang, I. Nopens, S. Van Hulle and P.A. Vanrolleghem, Nitrite effect on the phosphorus uptake activity of phosphate accumulating organisms (PAOs) in pilot-scale SBR and MBR reactors, Water SA 34 (2) (2008), pp. 249–260. View Record in Scopus | Cited By in Scopus (4) Smolders et al., 1994 G.J.F. Smolders, J. Van der Meij, M.C.M. Van Loosdrecht and J.J. Heijnen, Stoichiometric model of the aerobic metabolism of the biological phosphorus removal process, Biotechnology and Bioengineering 44 (7) (1994), pp. 837–848. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (158) Vadivelu et al., 2006a V.M. Vadivelu, J. Keller and Z. Yuan, Effect of free ammonia and free nitrous acid concentration on the anabolic and catabolic processes of an enriched Nitrosomonas culture, Biotechnology and Bioengineering 95 (5) (2006), pp. 830–839. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (25) Vadivelu et al., 2006b V.M. Vadivelu, Z. Yuan, C. Fux and J. Keller, The inhibitory effects of free nitrous acid on the energy generation and growth processes of an enriched Nitrobacter culture, Environmental Science & Technology 40 (14) (2006), pp. 4442–4448. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (29) Vadivelu et al., 2007 V.M. Vadivelu, J. Keller and Z. Yuan, Free ammonia and free nitrous acid inhibition on the anabolic and catabolic processes of Nitrosomonas and Nitrobacter, Water Science and Technology 56 (7) (2007), pp. 89–97. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (14) Weon et al., 2002 S.Y. Weon, C.W. Lee, S.I. Lee and B. Koopman, Nitrite inhibition of aerobic growth of Acinetobacter sp, Water Research 36 (18) (2002), pp. 4471–4476. Article | PDF (122 K) | View Record in Scopus | Cited By in Scopus (19) Wong et al., 2004 M.T. Wong, F.M. Tan, W.J. Ng and W.T. Liu, Identification and occurrence of tetrad-forming Alphaproteobacteria in anaerobic-aerobic activated sludge processes, Microbiology-Sgm 150 (2004), pp. 3741–3748. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (60) Yang et al., 2007 Q. Yang, Y.Z. Peng, X.H. Liu, W. Zeng, T. Mino and H. Satoh, Nitrogen removal via nitrite from municipal wastewater at low temperatures using real-time control to optimize nitrifying communities, Environmental Science & Technology 41 (23) (2007), pp. 8159–8164. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (35) Yang, 1985 T.Y. Yang, Mechanism of nitrite inhibition of cellular respiration in Pseudomonas aeruginosa, Current Microbiology 12 (1) (1985), pp. 35–39. Full Text via CrossRef Yarbrough et al., 1980 J.M. Yarbrough, J.B. Rake and R.G. Eagon, Bacterial inhibitory effects of nitrite inhibition of active transport, but not of group translocation, and of intracellular enzymes, Applied and Environmental Microbiology 39 (4) (1980), pp. 831–834. View Record in Scopus | Cited By in Scopus (20) Yoshida et al., 2006 Y. Yoshida, K. Takahashi, T. Saito and K. Tanaka, The effect of nitrite on aerobic phosphate uptake and denitrifying activity of phosphate accumulating organisms, Water Science and Technology 53 (6) (2006), pp. 21–27. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (5) Zeng et al., 2003 R.J. Zeng, M.C.M. van Loosdrecht, Z. Yuan and J. Keller, Metabolic model for glycogen accumulating organisms in anaerobic/aerobic activated sludge systems, Biotechnology and Bioengineering 81 (1) (2003), pp. 92–105. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (64) Zhou et al., 2007 Y. Zhou, M. Pijuan and Z. Yuan, Free nitrous acid inhibition on anoxic phosphorus uptake and denitrification by poly-phosphate accumulating organisms, Biotechnology and Bioengineering 98 (2007), pp. 903–912. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (17) Zhou et al., 2008 Y. Zhou, M. Pijuan, R.J. Zeng and Z. Yuan, Free nitrous acid inhibition on nitrous oxide reduction by a denitrifying-enhanced biological phosphorus removal sludge, Environmental Science & Technology 42 (22) (2008), pp. 8260–8265. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (8)
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Additional Notes Published Online 13 January, 2010.

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2011 Collection
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