In situ profiling of microbial communities in full-scale aerobic sequencing batch reactors treating winery waste in Australia

Environmental Science and Technology

Volumn 45, Issue 20, 2011, Pages 8794-8803

  McIlroy, Simon J ^a   Speirs, Lachlan B M ^a   Tucci, Joseph ^a   Seviour, Robert J ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AUSTRALIA; CAPSULAR MATERIALS; EUROPAEA; IN-SITU; MICROBIAL COMMUNITIES; MOLECULAR METHODS; OPERATIONAL PERIODS; SEQUENCING BATCH REACTORS; SETTLEABILITY; TETRAD-FORMING ORGANISMS; THREE SYSTEMS; TREATMENT PLANTS; WINERY WASTES;

ACTIVATED SLUDGE PROCESS; MICROORGANISMS; WASTEWATER; WASTEWATER TREATMENT; WINE;

BATCH REACTORS;

NITROGEN; PHOSPHORUS;

ANOXIC CONDITIONS; BACTERIUM; BIOREACTOR; BREWING INDUSTRY; CHEMICAL OXYGEN DEMAND; INDUSTRIAL WASTE; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; WASTEWATER;

ALPHAPROTEOBACTERIA; ARTICLE; CHEMICAL OXYGEN DEMAND; FLUORESCENCE IN SITU HYBRIDIZATION; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCING BATCH REACTOR; WASTE; WINE INDUSTRY; ZOOGLOEA;

AEROBIOSIS; ALPHAPROTEOBACTERIA; AUSTRALIA; BIOREACTORS; WASTE DISPOSAL, FLUID; WINE; ZOOGLOEA;

AUSTRALIA;

AMARICOCCUS; CANDIDATUS ALYSIOSPHAERA; ZOOGLOEA;

EID: 80054692111     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es2018576     Document Type: Article

References (74)

1. Brito, A. G.; Peixoto, J.; Oliveira, J. M.; Oliveira, J. A.; Costa, C.; Nogueira, R.; Rodrigues, A. Brewery and winery wastewater treatment: some focal points of design and operation. In Utilization of by-products and treatment of waste in the food industry; Oreopoulou, V., Russ, W., Eds.; Springer: New York, 2007; Vol. 3, pp 109-131.
2. Eusébio, A.; Petruccioli, M.; Lageiro, M.; Federici, F.; Duarte, J. C. Microbial characterisation of activated sludge in jet-loop bioreactors treating winery wastewaters J. Ind. Microbiol. Biotechnol. 2004, 31 (1) 29-34
3. Eusebi, A. L.; Nardelli, P.; Gatti, G.; Battistoni, P.; Cecchi, F. From conventional activated sludge to alternate oxic/anoxic process: the optimization of winery wastewater treatment Water Sci. Technol. 2009, 60 (4) 1041-1048
4. Arvanitoyannis, I. S.; Ladas, D.; Mavromatis, A. Wine waste treatment methodology Int. J. Food Sci. Technol. 2006, 41 (10) 1117-1151
5. Frost, P.; Kumar, A.; Correll, R.; Quayle, W.; Kookana, R.; Christen, E.; Oemcke, D. Current practices for winery wastewater management and its reuse: an Australian industry survey Wine Ind. J. 2007, 22 (1) 40-46
6. Torrijos, M.; Moletta, R. Winery wastewater depollution by sequencing batch reactor Water Sci. Technol. 1997, 35 (1) 249-257
7. Seviour, R. J.; Nielsen, P. H. Microbial Ecology of Activated Sludge; IWA Publishing: London, 2010.
8. He, S.; McMahon, K. D. Microbiology of Candidatus Accumulibacter in activated sludge. Microb. Biotechnol. In press, doi: 10.1111/j.1751-7915.2011. 00248.x.
9. McMahon, K. D.; He, S.; Oehmen, A. The microbiology of phosphorus removal. In Microbial ecology of activated sludge; Seviour, R. J.; Nielsen, P. H., Eds.; IWA Publishing: London, 2010; pp 281-319.
10. Daims, H.; Wagner, M. The microbiology of nitrogen removal. In Microbial ecology of activated sludge; Seviour, R. J.; Nielsen, P. H., Eds.; IWA Publishing: London, 2010; pp 259-280.
11. Oehmen, A.; Lemos, P. C.; Carvalho, G.; Yuan, Z.; Keller, J.; Blackall, L. L.; Reis, M. A. M. Advances in enhanced biological phosphorus removal: from micro to macro scale Water Res. 2007, 41 (11) 2271-2300
12. Jobbágy, A.; Literáthy, B.; Tardy, G. Implementation of glycogen accumulating bacteria in treating nutrient-deficient wastewater Water Sci. Technol. 2002, 46 (1-2) 185-190
13. Gonzalez, J. M.; Jurado, V.; Laiz, L.; Zimmermann, J.; Hermosin, B.; Saiz-Jimenez, C. Pectinatus portalensis non. sp., a relatively fast-growing, coccoidal, novel Pectinatus species isolated from a wastewater treatment plant Antonie van Leeuwenhoek 2004, 86 (3) 241-248
14. Daims, H.; Stoecker, K.; Wagner, M. Fluorescence in situ hybridization for the detection of prokaryotes. In Molecular Microbial Ecology; Osborn, A. M.; Smith, C. J., Eds.; Taylor & Francis: New York, 2005; pp 213-239.
15. Kragelund, C.; Remesova, Z.; Nielsen, J.; Thomsen, T.; Eales, K.; Seviour, R.; Wanner, J.; Nielsen, P. Ecophysiology of mycolic acid-containing Actinobacteria (Mycolata) in activated sludge foams FEMS Microbiol. Ecol. 2007, 61 (1) 174-184
16. Amann, R. I.; Binder, B. J.; Olson, R. J.; Chisolm, S. W.; Devereux, R.; Stahl, D. A. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations Appl. Environ. Microbiol. 1990, 56 (6) 1919-1925
17. Daims, H.; Brühl, A.; Amann, R.; Schleifer, K.; Wagner, M. 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. 1999, 22 (3) 434-444
18. Wallner, G.; Amann, R.; Beisker, W. Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms Cytometry 1993, 14 (2) 136-143
19. Manz, W.; Amann, R.; Ludwig, W.; Wagner, M.; Scheifer, K.-H. Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions Syst. Appl. Microbiol. 1992, 15 (4) 593-600
20. Zilles, J.; Peccia, J.; Kim, M.; Hung, C.; Noguera, D. Involvement of Rhodocyclus -related organisms in phosphorus removal in full-scale wastewater treatment plants Appl. Environ. Microbiol. 2002, 68 (6) 2763-2769
21. Crocetti, G. R.; Hugenholtz, P.; Bond, P. L.; Schuler, A.; Keller, J.; Jenkins, D.; Blackall, L. L. Identification of polyphosphate-accumulating organisms and design of 16S rRNA-directed probes for their detection and quantitation Appl. Environ. Microbiol. 2000, 66 (3) 1175-1182
22. Rossello-Mora, R. A.; Wagner, M. The abundance of Zoogloea ramigera in sewage treatment plants Appl. Environ. Microbiol. 1995, 61 (2) 702-707
23. Hess, A.; Zarda, B.; Hahn, D.; Haner, A.; Stax, D.; Hohener, P.; Zeyer, J. In situ analysis of denitrifying toluene- and m-xylene-degrading bacteria in a diesel fuel-contaminated laboratory aquifer column Appl. Environ. Microbiol. 1997, 63 (6) 2136-41
24. Wagner, M.; Amann, R.; Kämpfer, P.; Assmus, B.; Hartmann, A.; Hutzler, P.; Springer, N.; Schleifer, K.-H. Identification and in situ detection of gram-negative filamentous bacteria in activated sludge Syst. Appl. Microbiol. 1994, 17 (3) 405-417
25. Kong, Y.; Ong, S. L.; Ng, W. J.; Liu, W.-T. Diversity and distribution of a deeply branched novel proteobacterial group found in anaerobic-aerobic activated sludge processes Environ. Microbiol. 2002, 4 (11) 753-757
26. Neef, A.; Witzenberger, R.; Kämpfer, P. Detection of sphingomonads and in situ identification in activated sludge using 16S rRNA-targeted oligonucleotide probes J. Ind. Microbiol. Biotechnol. 1999, 23 (4-5) 261-267
27. Wong, M.-T.; Tan, F. M.; Ng, W. J.; Liu, W.-T. Identification and occurrence of tetrad-forming Alphaproteobacteria in anaerobic-aerobic activated sludge processes Microbiology 2004, 150 (11) 3741-3748
28. Meyer, R. L.; Saunders, A. M.; Blackall, L. L. Putative glycogen-accumulating organisms belonging to the Alphaproteobacteria identified through rRNA-based stable isotope probing Microbiology 2006, 152 (2) 419-429
29. Nittami, T.; McIlroy, S.; Seviour, E. M.; Schroeder, S.; Seviour, R. J. Candidatus Monilibacter spp., common bulking filaments in activated sludge, are members of Cluster III Defluviicoccus Syst. Appl. Microbiol. 2009, 32 (7) 480-489
30. McIlroy, S.; Seviour, R. J. Elucidating further phylogenetic diversity among the Defluviicoccus -related glycogen-accumulating organisms in activated sludge Environ. Microbiol. Rep. 2009, 1 (6) 563-568
31. Maszenan, A.-M.; Seviour, R. J.; Patel, B. K.; Wanner, J. A fluorescently-labelled r-RNA targeted oligonucleotide probe for the in situ detection of G-bacteria of the genus Amaricoccus in activated sludge J. Appl. Microbiol. 2000, 88 (5) 826-835
32. Snaidr, I.; Beimfohr, C.; Levantesi, C.; Rossetti, S.; van der Waarde, J.; Geurkink, B.; Eikelboom, D.; Lemaitre, M.; Tandoi, V. Phylogenetic analysis and in situ identification of " Nostocoida limicola "-like filamentous bacteria in activated sludge from industrial wastewater treatment plants Water Sci. Technol. 2002, 46 (1-2) 99-104
33. Roller, C.; Wagner, M.; Amann, R.; Ludwig, W.; Schleifer, K.-H. In situ probing of Gram-positive bacteria with high DNA G + C content using 23S rRNA-targeted oligonucleotides Microbiology 1994, 140 (10) 2849-2858
34. Meier, H.; Amann, R.; Ludwig, W.; Schleifer, K. Specific oligonucleotide probes for in situ detection of a major group of Gram-positive bacteria with low DNA G + C content Syst. Appl. Microbiol. 1999, 22 (3) 186-196
35. Björnsson, L.; Hugenholtz, P.; Tyson, G. W.; Blackall, L. L. Filamentous Chloroflexi (green non-sulfur bacteria) are abundant in wastewater treatment processes with biological nutrient removal Microbiology 2002, 148 (8) 2309-2318
36. Gich, F.; Garcia-Gil, J.; Overmann, J. Previously unknown and phylogenetically diverse members of the green nonsulfur bacteria are indigenous to freshwater lakes Arch. Microbiol. 2001, 177 (1) 1-10
37. Beer, M.; Seviour, E. M.; Kong, Y.; Cunningham, M.; Blackall, L. L.; Seviour, R. J. 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. 2002, 207 (2) 179-183
38. Kragelund, C.; Levantesi, C.; Borger, A.; Thelen, K.; Eikelboom, D.; Tandoi, V.; Kong, Y.; van der Waarde, J.; Krooneman, J.; Rossetti, S.; Thomsen, T.; Nielsen, P. Identity, abundance and ecophysiology of filamentous Chloroflexi species present in activated sludge treatment plants FEMS Microbiol Ecol 2007, 59 (3) 671-682
39. Speirs, L.; Nittami, T.; McIlroy, S.; Schroeder, S.; Seviour, R. J. Filamentous bacterium Eikelboom type 0092 in activated sludge plants in Australia is a member of the phylum Chloroflexi Appl. Environ. Microbiol. 2009, 75 (8) 2446-52
40. Speirs, L. B. M.; McIlroy, S. J.; Petrovski, S.; Seviour, R. J. The activated sludge bulking filament Eikelboom morphotype 0914 is a member of the Chloroflexi Environ. Microbiol. Rep. 2011, 3 (2) 159-165
41. Kragelund, C.; Thomsen, T. R.; Mielczarek, A. T.; Nielsen, P. H. Eikelboom's morphotype 0803 in activated sludge belongs to the genus Caldilinea in the phylum Chloroflexi FEMS Microbiol. Ecol. 2011, 76 (3) 451-62
42. Neef, A.; Amann, R.; Schlesner, H.; Schleifer, K.-H. Monitoring a widespread bacterial group: in situ detection of Planctomycetes with 16S rRNA-targeted probes Microbiology 1998, 144 (12) 3257-3266
43. Manz, W.; Amann, R.; Ludwig, W.; Vancanneyt, M.; Schleifer, K. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment Microbiology 1996, 142 (5) 1097-1106
44. Weller, R.; Glöckner, F.; Amann, R. 16S rRNA-targeted oligonucleotide probes for the in situ detection of members of the phylum Cytophaga-Flavobacterium-Bacteroides Syst. Appl. Microbiol. 2000, 23 (1) 107-114
45. Hugenholtz, P.; Tyson, G. W.; Webb, R. I.; Wagner, A. M.; Blackall, L. L. Investigation of candidate division TM7, a recently recognized major lineage of the domain bacteria with no known pure-culture representatives Appl. Environ. Microbiol. 2001, 67 (1) 411-419
46. Kawaharasakia, M.; Tanakab, H.; Kanagawaa, T.; Nakamuraa, K. In situ identification of polyphosphate-accumulating bacteria in activated sludge by dual staining with rRNA-targeted oligonucleotide probes and 4′,6- diamidino-2-phenylindol (DAPI) at a polyphosphate-probing concentration Water Res. 1999, 33 (1) 257-265
47. Ostle, A.; Holt, J. Nile blue A as a fluorescent stain for poly-beta-hydroxybutyrate Appl. Environ. Microbiol. 1982, 44 (1) 238-241
48. Ahn, J.; Schroeder, S.; Beer, M.; McIlroy, S.; Bayly, R. C.; May, J. W.; Vasiliadis, G.; Seviour, R. J. Ecology of the microbial community removing phosphate from wastewater under continuously aerobic conditions in a sequencing batch reactor Appl. Environ. Microbiol. 2007, 73 (7) 2257-2270
49. Jenkins, D.; Richard, M. G.; Daigger, G. T. Manual on the causes and control of activated sludge bulking, foaming and other solids separation problems, 3 rd ed.; CRC Press LLC: London, England, 2004.
50. McIlroy, S.; Porter, K.; Seviour, R. J.; Tillett, D. Simple and safe method for simultaneous isolation of microbial RNA and DNA from problematic populations Appl. Environ. Microbiol. 2008, 74 (21) 6806-6807
51. Tillett, D.; Neilan, B. A. Xanthogenate nucleic acid isolation from cultured and environmental Cyanobacteria J. Phycol. 2000, 36 (1) 251-258
52. Lane, D. 16S/23S rRNA sequencing. In Modern microbial methods: Nucleic acid techniques in bacterial systematics; Stackebrandt, E.; Goodfellow, M., Eds.; John Wiley & Sons: England, 1991; pp 115-175.
53. Maszenan, A.; Seviour, R.; Patel, B.; Rees, G.; McDougall, B. Amaricoccus gen. nov., a Gram-negative coccus occurring in regular packages or tetrads, isolated from activated sludge biomass, and descriptions of Amaricoccus veronensis sp. nov., Amaricoccus tamworthensis sp. nov., Amaricoccus macauensis sp. nov., and Amaricoccus kaplicensis sp. nov Int. J. Syst. Bacteriol. 1997, 47 (3) 727-734
54. McIlroy, S.; Hoefel, D.; Schroeder, S.; Ahn, J.; Tillett, D.; Saint, C.; Seviour, R. FACS enrichment and identification of floc-associated alphaproteobacterial tetrad-forming organisms in an activated sludge community FEMS Microbiol. Lett. 2008, 285 (1) 130-135
55. Kragelund, C.; Kong, Y.; van der Waarde, J.; Thelen, K.; Eikelboom, D.; Tandoi, V.; Thomsen, T.; Nielsen, P. Ecophysiology of different filamentous Alphaproteobacteria in industrial wastewater treatment plants Microbiology 2006, 152 (10) 3003-3012
56. Levantesi, C.; Beimfohr, C.; Geurkink, B.; Rossetti, S.; Thelen, K.; Krooneman, J.; Snaidr, J.; van der Waarde, J.; Tandoi, V. Filamentous Alphaproteobacteria associated with bulking in industrial wastewater treatment plants Syst. Appl. Microbiol. 2004, 27 (6) 716-727
57. Yilmaz, L. S.; Parnerkar, S.; Noguera, D. R. mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization Appl. Environ. Microbiol. 2011, 77 (3) 1118-22
58. McIlroy, S. J.; Tillett, D.; Petrovski, S.; Seviour, R. J. Non-target sites with single nucleotide insertions or deletions are frequently found in 16S rRNA sequences and can lead to false positives in fluorescence in situ hybridization (FISH) Environ. Microbiol. 2011, 13 (1) 38-47
59. Falvo, A.; Levantesi, C.; Rossetti, S.; Seviour, R.; Tandoi, V. Synthesis of intracellular storage polymers by Amaricoccus kaplicensis, a tetrad forming bacterium present in activated sludge J. Appl. Microbiol. 2001, 91 (2) 299-305
60. Maszenan, A.; Seviour, R.; Patel, B.; Janssen, P.; Wanner, J. Defluvicoccus vanus gen. nov., sp. nov., a novel Gram-negative coccus/coccobacillus in the Alphaproteobacteria from activated sludge Int. J. Syst. Evol. Microbiol. 2005, 55 (5) 2105-2111
61. Seviour, R. J.; Maszenan, A. M.; Soddell, J. A.; Tandoi, V.; Patel, B. K. C.; Kong, Y.; Schumann, P. Microbiology of the 'G-bacteria' in activated sludge Environ. Microbiol. 2000, 2 (6) 581-593
62. Liu, W. T.; Mino, T.; Nakamura, K.; Matsuo, T. Glycogen accumulating population and its anaerobic substrate uptake in anaerobic-aerobic activated sludge without biological phosphorus removal Water Res. 1996, 30 (1) 75-82
63. Kong, Y. H.; Beer, M.; Rees, G. N.; Seviour, R. J. Functional analysis of microbial communities in aerobic-anaerobic sequencing batch reactors fed with different phosphorus/carbon (P/C) ratios Microbiology 2002, 148 (8) 2299-2307
64. Mino, T.; Liu, W.-T.; Kurisu, F.; Matsuo, T. Modelling glycogen storage and denitrification capability of microorganisms in enhanced biological phosphate removal processes Water Sci. Technol. 1995, 31 (2) 25-34
65. McIlroy, S. J.; Nittami, T.; Seviour, E. M.; Seviour, R. J. Filamentous members of cluster III Defluviicoccus have the in situ phenotype expected of a glycogen accumulating organism in activated sludge FEMS Microbiol. Ecol. 2010, 74 (1) 248-256
66. Pisco, A. R.; Bengtsson, S.; Werker, A.; Reis, M. A. M.; Lemos, P. C. Community structure evolution and enrichment of glycogen-accumulating organisms producing polyhydroxyalkanoates from fermented molasses Appl. Environ. Microbiol. 2009, 75 (14) 4676-86
67. Bengtsson, S.; Werker, A.; Welander, T. Production of polyhydroxyalkanoates by glycogen accumulating organisms treating a paper mill wastewater Water Sci. Technol. 2008, 58 (2) 323-330
68. Burow, L. C.; Mabbett, A. N.; Borras, L.; Blackall, L. L. Anaerobic central metabolic pathways active during polyhydroxyalkanoate production in uncultured cluster 1 Defluviicoccus enriched in activated sludge communities FEMS Microbiol. Lett. 2009, 298 (1) 79-84
69. Oehmen, A.; Zeng, R.; Saunders, A.; Blackall, L.; Keller, J.; Yuan, Z. Anaerobic and aerobic metabolism of glycogen-accumulating organisms selected with propionate as the sole carbon source Microbiology 2006, 152 (9) 2767-2778
70. Dai, Y.; Yuan, Z.; Wang, X.; Oehmen, A.; Keller, J. Anaerobic metabolism of Defluviicoccus vanus related glycogen accumulating organisms (GAOs) with acetate and propionate as carbon sources Water Res. 2007, 41 (9) 1885-1896
71. Cech, J. S.; Hartman, P. Competition between polyphosphate and polysaccharide accumulating bacteria in enhanced biological phosphate removal systems Water Res. 1993, 27 (7) 1219-1225
72. McIlroy, S. J. Phylogenetic diversity and ecophysiology of alphaproteobacterial glycogen accumulating organisms in enhanced biological phosphorus removal activated sludge systems. Ph.D. Thesis, La Trobe University, Bendigo, 2010.
73. Kessler, B.; Witholt, B. Factors involved in the regulatory network of polyhydroxyalkanoate metabolism J. Biotechnol. 2001, 86 (2) 97-104
74. Norberg, A. B.; Enfors, S.-O. Production of extracellular polysaccharide by Zoogloea ramigera Appl. Environ. Microbiol. 1982, 44 (5) 1231-1237