Biofilm stratification during simultaneous nitrification and denitrification (SND) at a biocathode

Virdis, Bernardino, Read, Suzanne T., Rabaey, Korneel, Rozendal, Rene A., Yuan, Zhiguo and Keller, Jurg (2011) Biofilm stratification during simultaneous nitrification and denitrification (SND) at a biocathode. Bioresource Technology, 102 1: 334-341. doi:10.1016/j.biortech.2010.06.155


Author Virdis, Bernardino
Read, Suzanne T.
Rabaey, Korneel
Rozendal, Rene A.
Yuan, Zhiguo
Keller, Jurg
Title Biofilm stratification during simultaneous nitrification and denitrification (SND) at a biocathode
Journal name Bioresource Technology   Check publisher's open access policy
ISSN 0960-8524
1873-2976
Publication date 2011-01
Year available 2010
Sub-type Article (original research)
DOI 10.1016/j.biortech.2010.06.155
Volume 102
Issue 1
Start page 334
End page 341
Total pages 8
Editor A. Pandey
C. Larroche
S. C. Ricke
Place of publication Amsterdam, The Netherlands
Publisher Elsevier
Collection year 2011
Language eng
Abstract The aeration of the cathode compartment of bioelectrochemical systems (BESs) was recently shown to promote simultaneous nitrification and denitrification (SND). This study investigates the cathodic metabolism under different operating conditions as well as the structural organization of the cathodic biofilm during SND. Results show that a maximal nitrogen removal efficiency of 86.9 ± 0.5%, and a removal rate of 3.39 ± 0.08 mg N L−1 h−1 could be achieved at a dissolved oxygen (DO) level of 5.73 ± 0.03 mg L−1 in the catholyte. The DO levels used in this study are higher than the thresholds previously reported as detrimental for denitrification. Analysis of the cathodic half-cell potential during batch tests suggested the existence of an oxygen gradient within the biofilm while performing SND. FISH analysis corroborated this finding revealing that the structure of the biofilm included an outer layer occupied by putative nitrifying organisms, and an inner layer where putative denitrifying organisms were most dominant. To our best knowledge this is the first time that nitrifying and denitrifying microorganisms are simultaneously observed in a cathodic biofilm.
Keyword Bioelectrochemical systems
Denitrification
Cathodic process
Microbial fuel cell
Nitrification
References Bock et al., 1995 E. Bock, I. Schmidt, R. Stuven and D. Zart, Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium or hydrogen as electron-donors and nitrite as electron-acceptor, Archives of Microbiology 163 (1) (1995), pp. 16–20. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (172) Chen et al., 2006 F. Chen, Q. Xia and L.K. Ju, Competition between oxygen and nitrate respirations in continuous culture of Pseudomonas aeruginosa performing aerobic denitrification, Biotechnology and Bioengineering 93 (6) (2006), pp. 1069–1078. View Record in Scopus | Cited By in Scopus (9) Clauwaert et al., 2007 P. Clauwaert, K. Rabaey, P. Aelterman, L. DeSchamphelaire, T.H. Pham, P. Boeckx, N. Boon and W. Verstraete, Biological denitrification in microbial fuel cells, Environmental Science and Technology 41 (9) (2007), pp. 3354–3360. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (80) Cournet et al., 2010 A. Cournet, M. Berge, C. Roques, A. Bergel and M.-L. Delia, Electrochemical reduction of oxygen catalyzed by Pseudomonas aeruginosa, Electrochimica Acta 55 (17) (2010), pp. 4902–4908. Article | PDF (774 K) | View Record in Scopus | Cited By in Scopus (0) Daims et al., 2006 H. Daims, S. Lucker and M. Wagner, Daime, a novel image analysis program for microbial ecology and biofilm research, Environmental Microbiology 8 (2) (2006), pp. 200–213. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (76) Hochstein et al., 1984 L.I. Hochstein, M. Betlach and G. Kritikos, The effect of oxygen on denitrification during steady-state growth of Paracoccus halodenitrificans, Archives of Microbiology 137 (1) (1984), pp. 74–78. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (31) Keller et al., 1997 J. Keller, K. Subramaniam, J. Gosswein and P.F. Greenfield, Nutrient removal from industrial wastewater using single tank sequencing batch reactors, Water Science and Technology 35 (6) (1997), pp. 137–144. Abstract | View Record in Scopus | Cited By in Scopus (56) Korner and Zumft, 1989 H. Korner and W.G. Zumft, Expression of denitrification enzymes in response to the dissolved-oxygen level and respiratory substrate in continuous culture of Pseudomonas stutzeri, Applied and Environmental Microbiology 55 (7) (1989), pp. 1670–1676. View Record in Scopus | Cited By in Scopus (114) Kuroda et al., 1996 M. Kuroda, T. Watanabe and Y. Umedu, Simultaneous oxidation and reduction treatments of polluted water by a bio-electro reactor, Water Science and Technology 34 (9) (1996), pp. 101–108. Abstract | View Record in Scopus | Cited By in Scopus (23) Lu et al., 2006 H. Lu, A. Oehmen, B. Virdis, J. Keller and Z. Yuan, Obtaining highly enriched cultures of Candidatus Accumulibacter phosphates through alternating carbon sources, Water Research 40 (20) (2006), pp. 3838–3848. Article | PDF (476 K) | View Record in Scopus | Cited By in Scopus (29) Manz et al., 1993 W. Manz, U. Szewzyk, P. Ericsson, R. Amann, K.H. Schleifer and T.A. Stenstrom, In-situ identification of bacteria in drinking-water and adjoining biofilms by hybridation with 16S-ribosomal-RNA-directed and 23S-ribosomal-RNA-directed fluorescent oligonucleotide probes, Applied and Environmental Microbiology 59 (7) (1993), pp. 2293–2298. View Record in Scopus | Cited By in Scopus (157) Meyer et al., 2005 R.L. Meyer, R.J.X. Zeng, V. Giugliano and L.L. Blackall, Challenges for simultaneous nitrification, denitrification, and phosphorus removal in microbial aggregates: mass transfer limitation and nitrous oxide production, Fems Microbiology Ecology 52 (3) (2005), pp. 329–338. Article | PDF (517 K) | Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (19) Munch et al., 1996 E.V. Munch, P. Lant and J. Keller, Simultaneous nitrification and denitrification in bench-scale sequencing batch reactors, Water Research 30 (2) (1996), pp. 277–284. Article | PDF (656 K) | View Record in Scopus | Cited By in Scopus (155) Pochana and Keller, 1999 K. Pochana and J. Keller, Study of factors affecting simultaneous nitrification and denitrification (SND), Water Science and Technology 39 (6) (1999), pp. 61–68. Abstract | View Record in Scopus | Cited By in Scopus (107) Pratt et al., 2003 S. Pratt, Z.G. Yuan, D. Gapes, M. Dorigo, R.J. Zeng and J. Keller, Development of a novel titration and off-gas analysis (TOGA) sensor for study of biological processes in wastewater treatment systems, Biotechnology and Bioengineering 81 (4) (2003), pp. 482–495. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (61) Rabaey et al., 2005 K. Rabaey, N. Boon, M. Hofte and W. Verstraete, Microbial phenazine production enhances electron transfer in biofuel cells, Environmental Science and Technology 39 (9) (2005), pp. 3401–3408. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (126) Rabaey et al., 2007 K. Rabaey, J. Rodriguez, L.L. Blackall, J. Keller, P. Gross, D. Batstone, W. Verstraete and K.H. Nealson, Microbial ecology meets electrochemistry: electricity-driven and driving communities, ISME Journal 1 (1) (2007), pp. 9–18. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (69) Rabaey and Verstraete, 2005 K. Rabaey and W. Verstraete, Microbial fuel cells: novel biotechnology for energy generation, Trends in Biotechnology 23 (6) (2005), pp. 291–298. Article | PDF (284 K) | View Record in Scopus | Cited By in Scopus (254) Robertson and Kuenen, 1984 L.A. Robertson and J.G. Kuenen, Aerobic denitrification – a controversy revived, Archives of Microbiology 139 (4) (1984), pp. 351–354. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (100) Rozendal et al., 2009 R.A. Rozendal, E. Leone, J. Keller and K. Rabaey, Efficient hydrogen peroxide generation from organic matter in a bioelectrochemical system, Electrochemistry Communications 11 (9) (2009), pp. 1752–1755. Article | PDF (249 K) | View Record in Scopus | Cited By in Scopus (10) Schmidt et al., 2003 I. Schmidt, O. Sliekers, M. Schmid, E. Bock, J. Fuerst, J.G. Kuenen, M.S.M. Jetten and M. Strous, New concepts of microbial treatment processes for the nitrogen removal in wastewater, Fems Microbiology Reviews 27 (4) (2003), pp. 481–492. Article | PDF (481 K) | Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (110) Schmidt et al., 2004 I. Schmidt, R.J.M. van Spanning and M.S.M. Jetten, Denitrification and ammonia oxidation by Nitrosomonas europaea wild-type, and NirK- and NorB-deficient mutants, Microbiology-Sgm 150 (2004), pp. 4107–4114. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (36) Shaw et al., 2006 L.J. Shaw, G.W. Nicol, Z. Smith, J. Fear, J.I. Prosser and E.M. Baggs, Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway, Environmental Microbiology 8 (2) (2006), pp. 214–222. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (34) Su et al., 2001 J.J. Su, B.Y. Liu and C.Y. Liu, Comparison of aerobic denitrification under high oxygen atmosphere by Thiosphaera pantotropha ATCC 35512 and Pseudomonas stutzeri SU2 newly isolated from the activated sludge of a piggery wastewater treatment system, Journal of Applied Microbiology 90 (3) (2001), pp. 457–462. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (28) Takaya et al., 2003 N. Takaya, M.A. Catalan-Sakairi, Y. Sakaguchi, I. Kato, Z. Zhou and H. Shoun, Aerobic denitrifying bacteria that produce low levels of nitrous oxide, Applied and Environmental Microbiology 69 (6) (2003), pp. 3152–3157. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (48) Third et al., 2003 K.A. Third, N. Burnett and R. Cord-Ruwisch, Simultaneous nitrification and denitrification using stored substrate (PHB) as the electron donor in an SBR, Biotechnology and Bioengineering 83 (6) (2003), pp. 706–720. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (43) Uemoto and Saiki, 2000 H. Uemoto and H. Saiki, Distribution of Nitrosomonas europaea and Paracoccus denitrificans immobilized in tubular polymeric gel for nitrogen removal, Applied and Environmental Microbiology 66 (2) (2000), pp. 816–819. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (10) Van Loosdrecht and Jetten, 1998 M.C.M. Van Loosdrecht and M.S.M. Jetten, Microbiological conversions in nitrogen removal, Water Science and Technology 38 (1) (1998), pp. 1–7. Abstract | View Record in Scopus | Cited By in Scopus (33) Virdis et al., 2010 B. Virdis, K. Rabaey, R.A. Rozendal, Z. Yuan and J. Keller, Simultaneous nitrification, denitrification and carbon removal in microbial fuel cells, Water Research 44 (9) (2010), pp. 2970–2980. Article | PDF (814 K) | View Record in Scopus | Cited By in Scopus (0) Virdis et al., 2008 B. Virdis, K. Rabaey, Z. Yuan and J. Keller, Microbial fuel cells for simultaneous carbon and nitrogen removal, Water Research 42 (12) (2008), pp. 3013–3024. Article | PDF (1020 K) | View Record in Scopus | Cited By in Scopus (20) Virdis et al., 2009 B. Virdis, K. Rabaey, Z.G. Yuan, R.A. Rozendal and J. Keller, Electron fluxes in a microbial fuel cell performing carbon and nitrogen removal, Environmental Science and Technology 43 (13) (2009), pp. 5144–5149. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (6) Wrage et al., 2001 N. Wrage, G.L. Velthof, M.L. van Beusichem and O. Oenema, Role of nitrifier denitrification in the production of nitrous oxide, Soil Biology and Biochemistry 33 (12–13) (2001), pp. 1723–1732. Article | PDF (277 K) | View Record in Scopus | Cited By in Scopus (232) Yilmaz et al., 2008 G. Yilmaz, R. Lemaire, J. Keller and Z. Yuan, Simultaneous nitrification, denitrification, and phosphorus removal from nutrient-rich industrial wastewater using granular sludge, Biotechnology and Bioengineering 100 (3) (2008), pp. 529–541. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (13) Yoo et al., 1999 H. Yoo, K.-H. Ahn, H.-J. Lee, K.-H. Lee, Y.-J. Kwak and K.-G. Song, Nitrogen removal from synthetic wastewater by simultaneous nitrification and denitrification (SND) via nitrite in an intermittently-aerated reactor, Water Research 33 (1) (1999), pp. 145–154. Article | PDF (880 K) | View Record in Scopus | Cited By in Scopus (106) Zumft, 1997 W.G. Zumft, Cell biology and molecular basis of denitrification, Microbiology and Molecular Biology Reviews 61 (4) (1997), pp. 533–616. View Record in Scopus | Cited By in Scopus (896)
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Document type: Journal Article
Sub-type: Article (original research)
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