Characterization of the denitrification-associated phosphorus uptake properties of "Candidatusaccumulibacter phosphatis" clades in sludge subjected to enhanced biological phosphorus removal

Applied and Environmental Microbiology

Volumn 79, Issue 6, 2013, Pages 1969-1979

  Kim, Jeong Myeong ^a   Lee, Hyo Jung ^a   Lee, Dae Sung ^b   Jeon, Che Ok ^a  

^a Chung Ang University   (South Korea)

^b Kyungpook National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; ACCUMULIBACTER; ASSOCIATED BACTERIA; BATCH EXPERIMENTS; COMPETIBACTER; ENHANCED BIOLOGICAL PHOSPHORUS REMOVAL; NITRATE CONCENTRATION; NITRATE REDUCTION; NITRATE-REDUCING BACTERIA; PHOSPHORUS UPTAKE; POLYPHOSPHATES; RELATIVE ABUNDANCE; SEQUENCING BATCH REACTORS; STEPWISE INCREASE; UPTAKE PROPERTIES;

BACTERIA; DENITRIFICATION; EXPERIMENTS; NITRATES; RNA; WASTEWATER TREATMENT;

PHOSPHORUS;

ACETIC ACID DERIVATIVE; BACTERIAL DNA; PHOSPHORUS; RIBOSOME DNA; RNA 16S;

ACCLIMATION; ANOXIC CONDITIONS; BACTERIUM; DENITRIFICATION; NITRATE; NITRITE; NUTRIENT UPTAKE; OXIC CONDITIONS; PHOSPHORUS; POLLUTANT REMOVAL; RELATIVE ABUNDANCE; SLUDGE;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; BETAPROTEOBACTERIA; BIOREACTOR; BIOTA; CHEMISTRY; CLUSTER ANALYSIS; DENITRIFICATION; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEWAGE;

ACETATES; AEROBIOSIS; ANAEROBIOSIS; BETAPROTEOBACTERIA; BIOREACTORS; BIOTA; CLUSTER ANALYSIS; DENITRIFICATION; DNA, BACTERIAL; DNA, RIBOSOMAL; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHOSPHORUS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEWAGE;

EID: 84874816824     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03464-12     Document Type: Article

References (59)

1. Mino T, Van Loosdrecht MCM, Heijnen JJ.1998. Microbiology and biochemistry of the enhanced biological phosphate removal process. Wa-ter Res.32:3193-3207.
2. Albertsen M, Hansen LBS, Saunders AM, Nielsen PH, Nielsen KL.2012. A metagenome of a full-scale microbial community carrying out enhanced biological phosphorus removal. ISME J.6:1094-1106.
3. Bond PL, Hugenholtz P, Keller J, Blackall LL.1995. Bacterial commu-nity structures of phosphate-removing and non-phosphate-removing ac-tivated sludges fromsequencing batch reactors. Appl. Environ.Microbiol. 61:1910-1916.
4. Crocetti GR, Hugenholtz P, Bond PL, Schuler A, Keller J, Jenkins D,Blackall LL.2000. Identification of polyphosphate-accumulating organ-isms and design of 16S rRNA-directed probes for their detection and quantitation. Appl. Environ. Microbiol.66:1175-1182.
5. He S, Gu AZ, McMahon KD.2008. Progress toward understanding the distribution of accumulibacter among full-scale enhanced biological phosphorus removal systems. Microb. Ecol.55:229-236.
6. Hesselmann RPX, Werlen C, Hahn D, van der Meer JR, Zehnder AJB.1999. Enrichment, phylogenetic analysis anddetectionof a bacteriumthat performs enhanced biological phosphate removal in activated sludge.Syst. Appl. Microbiol.22:454-465.
7. Jeon CO, Lee DS, Park JM. 2003. Microbial communities in activated sludge performing enhancedbiological phosphorus removal ina sequenc-ing batch reactor. Water Res.37:2195-2205.
8. Kong Y, Nielsen JL, Nielsen PH.2004. Microautoradiographic study of Rhodocyclus-related polyphosphate-accumulating bacteria in full-scale enhanced biological phosphorus removal plants. Appl. Environ. Micro-biol.70:5383-5390.
9. Lee N, Nielsen PH, Aspegren H, Henze M, Schleifer KH, Jansen JL.2003. Long-termpopulation dynamics and in situ physiology in activated sludge systems with enhanced biological phosphorus removal operated with and without nitrogen removal. Syst. Appl. Microbiol.26:211-227.
10. Liu W-T, Nielsen AT, 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.
11. Zilles JL, Peccia J, Kim M-W, Hung C-H, Noguera DR.2002. Involve-ment ofRhodocyclus-related organisms in phosphorus removal in full-scale wastewater treatment plants. Appl. Environ. Microbiol. 68:2763-2769.
12. Carvalho G, Lemos PC, Oehmen A, Reis MAM.2007. Denitrifying phosphorus removal: linking the process performance with the microbial community structure. Water Res.41:4383-4396.
13. Garcia Martin H, Ivanova N, Kunin V, Warnecke F, Barry KW,McHardy AC, Yeates C, He S, Salamov AA, Szeto E, Dalin E, Putnam NH, Shapiro HJ, Pangilinan JL, Rigoutsos I, Kyrpides NC, Blackall LL,MaMahon KD, Hugenholtz P.2006. Metagenomic analysis of two en-hanced biological phosphorus removal (EBPR) sludge communities. Nat.Biotechnol.24:1263-1269.
14. He S, Gu AZ, McMahon KD.2006. Fine-scale differences between Ac-cumulibacter-like bacteria in enhanced biological phosphorus removal activated sludge. Water Sci. Technol.54:111-117.
15. Kim JM, Lee HJ, Kim SY, Song JJ, Park W, Jeon CO.2010. Analysis of the fine-scale population structure of "CandidatusAccumulibacter phos-phatis" in enhanced biological phosphorus removal sludge, using fluores-cence in situ hybridization and flow cytometric sorting. Appl. Environ.Microbiol.76:3825-3835.
16. Kong YH, Ong SL, Ng WJ, Liu WT.2002. Diversity and distribution of a deeply branched novel proteobacterial group found in anaerobic-aerobic activated sludge processes. Environ. Microbiol.4:753-757.
17. Wilmes P, Andersson AF, Lefsrud MG, Wexler M, Shah M, Zhang B, Hettich RL, Bond PL, Verberkmoes NC, Banfield JF.2008. Community proteogenomics highlights microbial strain-variant protein expression within activated sludge performing enhanced biological phosphorus re-moval. ISME J.2:853-864.
18. McMahon KD, Dojka MA, Pace NR, Jenkins D, Keasling JD.2002.Polyphosphate kinase fromactivated sludge performing enhancedbiolog-ical phosphorus removal. Appl. Environ. Microbiol.68:4971-4978.
19. He S, Gall DL, McMahon KD.2007. "CandidatusAccumulibacter"population structure in enhanced biological phosphorus removal sludges as revealed by polyphosphate kinase genes. Appl. Environ. Microbiol.73:5865-5874.
20. Peterson SB, Warnecke F, Madejska J, McMahon KD, Hugenholtz P.2008. Environmental distribution and population biology of the genus Accumulibacter, a primary agent of biological phosphorus removal in ac-tivated sludge. Environ. Microbiol.10:2692-2703.
21. Ahn J, Daidou T, Tsuneda S, Hirata A.2002. Characterization of deni-trifying phosphate-accumulating organisms cultivated chain reactor-denaturing gradient gel electrophoresis assay. Water Res.36:403-412.
22. Dabert P, Sialve B, Delgenés JP, Moletta R, Godon JJ.2001. Character-isation of the microbial 16S rDNA diversity of an aerobic phosphorus-removal ecosystemandmonitoring of its transition to nitrate respiration.Appl. Microbiol. Biotechnol.55:500-509.
23. Kerrn-Jespersen JP, HenzeM.1993. Biological phosphorus uptake under anoxic and aerobic conditions. Water Res.27:617-624.
24. Oehmen A, Lemos PC, Carvalho G, Yuan ZG, Keller J, Blackall LL, Reis MAM.2007. Advances in enhanced biological phosphorus removal: from micro to macro scale. Water Res.41:2271-2300.
25. Zeng RJ, Saunders AM, Yuan Z, Blackall LL, Keller J.2003. Identifica-tion and comparison of aerobic and denitrifying polyphosphate-accumulating organisms. Biotechnol. Bioeng.83:140-148.
26. Guisasola A, Qurie M, Vargas MM, Casas C, Baeza JA.2009. Failure of an enriched nitrite-DPAO population to use nitrate as an electron accep-tor. Process Biochem.44:689-695.
27. Flowers JJ, He S, Yilmaz S, Noguera DR, McMahon KD.2009. Deni-trificationcapabilities of twobiological phosphorus removal sludges dom-inated by different 'CandidatusAccumulibacter' clades. Environ. Micro-biol. Rep.1:583-588.
28. Oehmen A, Carvalho G, Freitas F, Reis MAM.2010. Assessing the abundance and activity of denitrifying polyphosphate accumulating or-ganisms throughmolecular and chemical techniques.Water Sci. Technol.61:2061-2068.
29. Jeon CO, Park JM.2000. Enhanced biological phosphorus removal in a sequencing batch reactor supplied with glucose as a sole carbon source.Water Res.34:2160-2170.
30. Lane DJ.1991. 16S/23S rRNA sequencing, p 115-147.InStackebrandt E,GoodfellowM(ed), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Inc, New York, NY.
31. Lu S, Park M, Ro HS, Lee DS, Park W, Jeon CO.2006. Analysis of microbial communities using culture-dependent and culture-independent approaches in an anaerobic/aerobic SBR reactor. J. Micro-biol.44:155-161.
32. Jeon CO, Park W, Padmanabhan P, DeRito C, Snape JR, Madsen EL.2003. Discovery of a previously undescribed bacterium with distinctive dioxygenase that is responsible for in situbiodegradation in contaminated sediment. Proc. Natl. Acad. Sci. U. S. A.100:13591-13596.
33. Huber T, Faulkner G, Hugenholtz P.2004. Bellerophon: a program to detect chimeric sequences inmultiple sequence alignments. Bioinformat-ics20:2317-2319.
34. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM,PhanR, AndersenGL.2006. NAST: amultiple sequence alignment server for comparative analysis of 16S rRNAgenes.NucleicAcids Res.34:W394-W399. doi:10.1093/nar/gkl244.
35. Felsenstein J.2002. PHYLIP (phylogeny inference package), version 3.6a.Department of Genetics, University of Washington, Seattle, WA.
36. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S,Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH.2004. ARB: a software environment for sequence data. Nucleic Acids Res.32:1363-1371.
37. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM.2009.The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145. doi:10.1093/nar/gkn879.
38. Hugenholtz P, Tyson GW, Blackall LL.2002. Design and evaluation of 16S rRNA-targeted oligonucleotide probe for fluorescencein situhybrid-ization. Methods Mol. Biol.179:29-42.
39. Amann RI, Ludwig W, Schleifer KH.1995. Phylogenetic identification andin situ detection of individual microbial cells without cultivation.Microbiol. Rev.59:143-169.
40. Daims H, Brühl A, Amann R, Schleifer KH, Wagner M.1999. The domain-specific probe EUB338 is insufficient for the detection of all Bac-teria: development and evaluation of a more comprehensive probe. Syst.Appl. Microbiol.22:434-444.
41. Kim JM, Lee HJ, Lee DS, Lee K, Jeon CO.2011. Identification of a novel subgroup of uncultured gammaproteobacterial glycogen-accumulating organisms in enhanced biological phosphorus removal sludge. Microbi-ology157:2287-2296.
42. Lee N, Nielsen PH, Andreasen KH, Juretschko S, Nielsen JL, Schleifer KH, Wagner M.1999. Combination of fluorescent in situ hybridization andmicroautoradiography-anewtool for structure-functionanalyses in microbial ecology. Appl. Environ. Microbiol.65:1289-1297.
43. Jeon CO, Lee DS, Lee MW, Park JM.2001. Enhanced biological phos-phorus removal in an anaerobic-aerobic sequencing batch reactor: effect of pH. Water Environ. Res.34:301-306.
44. Lee DS, Jeon CO, Park JM.2001. Biological nitrogen removal with enhanced phosphate uptake in a sequencing batch reactor using single sludge system. Water Res.35:3968-3976.
45. McMahon KD, Yilmaz S, He S, Gall DL, Jenkins D, Keasling JD.2007.Polyphosphate kinase genes from full-scale activated sludge plants. Appl.Microbiol. Biotechnol.77:167-173.
46. Ahn J, Schroeder S, Beer M, McIlroy S, Bayly RC, May JW, Vasiliadis G, Seviour RJ.2007. Ecology of the microbial community removing phosphate from wastewater under continuously aerobic conditions in a sequencing batch reactor. Appl. Environ. Microbiol.73:2257-2270.
47. Ahn J, Daidou T, Tsuneda S, Hirata A.2001. Metabolic behavior of denitrifying phosphate-accumulating organisms under nitrate and nitrite electron acceptor conditions. J. Biosci. Bioeng.92:442-446.
48. Kuba T, Wachtmeister A, Vanloosdrecht MCM, Heijnen JJ.1994. Effect of nitrate on phosphorus release in biological phosphorus removal sys-tems. Water Sci. Technol.30:263-269.
49. Meinhold J, Filipe CDM, Daigger GT, Isaacs S.1999. Characterization of the denitrifying fraction of phosphate accumulating organisms in bio-logical phosphate removal. Water Sci. Technol.39:31-42.
50. Zhou S, Zhang X, Feng L.2010. Effect of different types of electron acceptors on the anoxic phosphorus uptake activity of denitrifying phos-phorus removing bacteria. Bioresour. Technol.101:1603-1610.
51. Freitas F, Temudo M, Reis MAM.2005. Microbial population response to changes of the operating conditions in a dynamic nutrient-removal sequencing batch reactor. Bioproc. Biosyst. Eng.28:199-209.
52. Meinhold J, Arnold E, Isaacs S.1999. Effect of nitrite on anoxic phos-phate uptake in biological phosphorus removal activated sludge. Water Res.33:1871-1883.
53. Lanham AB, Moita R, Lemos PC, Reis MA.2011. Long-term operation of a reactor enriched inAccumulibacter clade IDPAOs: performancewith nitrate, nitrite and oxygen. Water Sci. Technol.63:352-359.
54. Ginige MP, Keller J, Blackall LL.2005. Investigation of an acetate-fed denitrifying microbial community by stable isotope probing, full-cycle rRNA analysis, and fluorescent in situ hybridization-microautoradiogra-phy. Appl. Environ. Microbiol.71:8683-8691.
55. Horn MA, Ihssen J, Matthies C, Schramm A, Acker G, Drake HL.2005. Dechloromonas denitrificanssp. nov.,Flavobacteriumdenitrificanssp. nov.,Paenibacillus anaericanussp. nov. andPaenibacillus terraestrain MH72,N2O-producing bacteria isolated from the gut of the earthwormAporrec-todea caliginosa. Int. J. Syst. Evol. Microbiol.55:1255-1265.
56. Kong Y, Xia Y, Nielsen JL, Nielsen PH.2006. Ecophysiology of a group of uncultured gammaproteobacterial glycogen-accumulating organisms in full-scale enhanced biological phosphorus removal wastewater treat-ment plants. Environ. Microbiol.8:479-489.
57. Lemaire R, Meyer R, Taske A, Crocetti GR, Keller J, Yuan Z.2006. Identifying causes for N 2O accumulation in a lab-scale sequencing batch reactor performing simultaneous nitrification, denitrification and phos-phorus removal. J. Biotechnol.122:62-72.
58. Oshiki M, Onuki M, Satoh H, Mino T.2008. PHA-accumulating mi-croorganisms in full-scale wastewater treatment plants. Water Sci. Tech-nol.58:13-20.
59. Zeng RJ, Yuan ZG, Keller J.2003. Enrichment of denitrifying glycogen-accumulating organisms in anaerobic/anoxic activated sludge system.Biotechnol. Bioeng.81:397-404.