Microbial community composition of polyhydroxyalkanoate-accumulating organisms in full-scale wastewater treatment plants operated in fully aerobic mode

Microbes and Environments

Volumn 28, Issue 1, 2013, Pages 96-104

  Oshiki, Mamoru ^a   Onuki, Motoharu ^b   Satoh, Hiroyasu ^b   Mino, Takashi ^b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Activated sludge; Fluorescence in situ hybridization; Microbial community composition; Polyhydroxyalkanoates accumulating organisms; Wastewater treatment plants

Indexed keywords

POLYHYDROXYALKANOIC ACID; RNA 16S;

AEROBIC METABOLISM; ALPHAPROTEOBACTERIA; ARTICLE; BETAPROTEOBACTERIA; CLASSIFICATION; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; RNA GENE; SEWAGE; WASTE WATER;

AEROBIOSIS; ALPHAPROTEOBACTERIA; BETAPROTEOBACTERIA; GENES, RRNA; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYHYDROXYALKANOATES; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEWAGE; WASTE DISPOSAL, FLUID; WASTE WATER;

EID: 84875178018     PISSN: 13426311     EISSN: 13474405     Source Type: Journal    
DOI: 10.1264/jsme2.ME12141     Document Type: Article

References (64)

1. Akarsubasi, A.T., O. Eyice, I. Miskin, I.M. Head, and T.P. Curtis. 2009. Effect of sludge age on the bacterial diversity of bench scale sequencing batch reactors. Environ. Sci. Technol. 43:2950-2956.
2. Altschul, S.F., T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Amann, R. 1995. In situ identification of microorganisms by whole cell hybridization with rRNA-targeted nucleic acid probes, p. 1-15. In A.D.L. Akkermans, D.J. van Elsas, and F.J. de Bruijn (ed.), Molecular Microbial Ecology Manual. Kluwer Academic Publishers, London.
4. American Public Health Association, American Water Works Association, Water Environment Federation. 2005. Standard methods for the examination of water and wastewater (21st Edition). American Public Health Association, Washington, D.C., USA.
5. Anderson, A.J., and E.A. Dawes. 1990. Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol. Rev. 54:450-472.
6. Beun, J.J., F. Paletta, M.C.M. Van Loosdrecht, and J.J. Heijnen. 2000. Stoichiometry and kinetics of poly-ß-hydroxybutyrate metabolism in aerobic, slow growing, activated sludge cultures. Biotechnol. Bioeng. 67:379-389.
7. Bjoörnsson, L., P. Hugenholtz, G.W. Tyson, and L.L. Blackall. 2002. Filamentous Chloroflexi (green non-sulfur bacteria) are abundant in wastewater treatment processes with biological nutrient removal. Microbiology 148:2309-2318.
8. Brandl, H., R.A. Gross, R.W. Lenz, R. Lloyd, and R.C. Fuller. 1991. The accumulation of poly(3-hydroxyalkanoates) in Rhodobacter Sphaeroides. Arch. Microbiol. 155:337-340.
9. Boon, N., W.D. Windt, W. Verstraete, and E.M. Top. 2002. Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiol. Ecol. 39:101-112.
10. Capon, R.J., R.W. Dunlop, E.L. Ghisalberti, and P.R. Jefferies. 1983. Poly-3-hydroxyalkanoates from marine and freshwater cyanobacteria. Phytochemistry 22:1181-1184.
11. Carucci, A., D. Dionisi, M. Majone, E. Rolle, and P. Smurra. 2001. Aerobic storage by activated sludge on real wastewater. Water Res. 35:3833-3844.
12. Cole, J.R., Q. Wang, E. Cardenas, et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145.
13. Crocetti, G.R., P. Hugenholtz, P.L. Bond, A. Schuler, J. Keller, D. Jenkins, and L.L. Blackall. 2000. Identification of polyphosphateaccumulating rganisms and design of 16S rRNA-directed probes for their detection and quantitation. Appl. Environ. Microbiol. 66:1175-1182.
14. Daims, H., A. Brühl, R. Amann, K.H. Schleifer, and M. Wagner. 1999. The domain-specific probe Eub338 is insufficient for the detection of all bacteria. development and evaluation of a more comprehensive probe set. Sys. Appl. Microbiol. 22:434-444.
15. Dionisi, D., M. Majone, G. Vallini, S.D. Gregorio, and M. Beccari. 2006. Effect of the applied organic load rate on biodegradable polymer production by mixed microbial cultures in a sequencing batch reactor. Biotechnol. Bioeng. 93:76-88.
16. Findlay, R.H., and D.C. White. 1983. Polymeric betahydroxyalkanoates from environmental samples and Bacillus megaterium. Appl. Environ. Microbiol. 45:71-78.
17. Freeman, C., M.A. Lock, and J. Marxsen. 1993. Poly-beta-hydroxy alkanoate and the support of river biofilm metabolism following radical changes in environmental conditions. Hydrobiologia 271:159-164.
18. Fukushima, T., N. Uda, M. Okamoto, M. Onuki, H. Satoh, and T. Mino. 2007. Abundance of Candidatus 'Accumulibacter phosphatis' in enhanced biological phosphorus removal activated sludge acclimatized with different carbon sources. Microbes Environ. 22:346-354.
19. Ginige, M.P., J. Keller, and L.L. Blackall. 2005. Investigation of an acetate-fed denitrifying microbial community by stable isotope probing, full-cycle rRNA analysis, and fluorescent in situ hybridization-microautoradiography. Appl. Environ. Microbiol. 71:8683-8691.
20. Gomez, J.G.C., M.F.A. Rodrigues, R.C.P. Alli, B.B. Torres, C.L. Bueno Netto, M.S. Oliveira, and L.F. da Silva. 1996. Evaluation of soil gram-negative bacteria yielding polyhydroxyalkanoic acids from carbohydrates and propionic acid. Appl. Microbiol. Biotechnol. 45:785-791.
21. Herron, J.S., J.D. King, and D.C. White. 1978. Recovery of poly-ß-hydroxybutyrate from estuarine microflora. Appl. Environ. Microbiol. 35:251-257.
22. Hesselmann, R.P., C. Werlen, D. Hahn, J. Roelof van Der Meer, and A.J.B. Zhender. 1999. Enrichment, phylogenetic analysis and detection of a bacterium that performs enhanced biological phosphate removal in activated sludge. Syst. Appl. Microbiol. 22:454-485.
23. Hiraishi, A., Y. Ueda, and J. Ishihara. 1998. Quinone profiling of bacterial communities in natural and synthetic sewage activated sludge for enhanced phosphate removal. Appl. Environ. Microbiol. 64:992-998.
24. Hvitved-Jacobsen, T., K. Raunkjær, and P.H. Nielsen. 1995. Volatile fatty acids and sulfide in pressure mains. Water Sci. Technol. 3:169-179.
25. Ibrahim, M.H.A., A. Willems, and A. Steinbüchel. 2010. Isolation and characterization of new poly(3HB)-accumulating star-shaped cell-aggregates-forming thermophilic bacteria. J. Appl. Microbiol.109:1579-1590.
26. Iwakaki, M., and A. Hiraishi. 1998. A new approach to numerical analyses of microbial quinone profiles in the environment. Microbes Environ. 13:67-76.
27. Johnson, K., Y. Jiang, R. Kleerebezem, G. Muyzer, and M.C.M. van Loosdrecht. 2009. Enrichment of a mixed bacterial culture with a high polyhydroxyalkanoate storage capacity. Biomacromolecules 10:670-676.
28. Karr, D.B., J.K. Waters, and A.D.W. Emerich. 1983. Analysis of poly-ß-hydroxybutyrate in Rhizobium japonicum bacteroids by ionexclusion high-pressure liquid chromatography and UV detection. Appl. Environ. Microbiol. 46:1339-1344.
29. Kadouri, D., E. Jurkevitch, and Y. Okon. 2005. Ecological and agricultural significance of bacterial polyhydroxyalkanoates. Crit. Rev. Microbiol. 31:55-67.
30. Kindaichi, T., T. Awata, Y. Suzuki, K. Tanabe, M. Hatamoto, N. Ozaki, and A. Ohashi. 2011. Enrichment using an up-flow column reactor and community structure of marine anammox bacteria from coastal sediment. Microbes Environ. 26:67-73.
31. Kitamura, S., and Y. Doi. 1994. Staining method of poly(3-hydroxyalkanoic acids) producing bacteria by Nile blue. Biotechnol. Tech. 8:345-350.
32. Kondo, T., Y. Ebie, S. Tsuneda, and Y. Inamori. 2007. Detection of Defluvicoccus-related glycogen-accumulating organisms in enhanced biological phosphorus removal processes. Microbes Environ. 22:190-195.
33. Kragelund, C., C. Levantesi, A. Borger, et al. 2007. Identity, abundance and ecophysiology of filamentous Chloroflexi species present in activated sludge treatment plants. FEMS Microbiol. Ecol. 59:671-682.
34. Lane, D.J. 1996. 16S/23S rRNA sequencing, p. 115-175. In E. Stackebrant, and M. Goodfellow (ed.), Nucleic Acid Techniques in Bacterial Systematics. John Wiley & Sons Ltd., London.
35. Lemos, P.C., C. Levantesi, L.S. Serafim, S. Rossetti, M.A.M. Reis, and V. Tandoi. 2008. Microbial characterization of polyhydroxyalkanoates storing populations selected under different operating conditions using a cell-sorting RT-PCR approach. Appl. Microbiol. Biotechnol. 78:351-360.
36. Lopez, N.I., M.E. Floccari, A. Steinbüchel, A.F. Garcia, and B.S. Mendez. 1995. Effect of poly(3-hydroxybutyrate) (PHB) content on the starvation-survival of bacteria in natural waters. FEMS Microbiol. Ecol. 16:95-102.
37. Ludwig, W., O. Strunk, R. Westram, et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
38. Manz, W., R. Amann, W. Ludwig, M. Wagner, and K.H. Schleifer. 1992. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15:593-600.
39. Manz, W., R. Amann, W. Ludwig, M. Vancanneyt, and K.H. Schleifer. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Bacteroidetes in the natural environment. Microbiology 142:1097-1106.
40. Matias, F., D. Bonatto, G. Padilla, M.F. de Andrade Rodrigues, and J.A.P. Henriques. 2009. Polyhydroxyalkanoates production by Actinobacteria isolated from soil. Can. J. Microbiol. 55:790-800.
41. Meier, H., R. Amann, W. Ludwig, and K.H. Schleifer. 1999. Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G+C content. Syst. Appl. Microbiol. 22:186-196.
42. Mino, T., M.C.M. Van Loosdrecht, and J.J. Heijnen. 1998. Microbiology and biochemistry of the enhanced biological phosphate removal process. Water Res. 32:3193-3207.
43. Neef, A., R. Witzenberger, and P. Kämpfer. 1999. Detection of Sphingomonads and in situ identification in activated sludge using 16S rRNA-targeted oligonucleotide probes. J. Ind. Microbiol. Biotech. 23:261-267.
44. Nielsen, A.T., W.T. Liu, C. Filipe, L.G. JR, S. Molin, and D.A. Stahl. 1999. Identification of a novel group of bacteria in sludge from a deteriorated biological phosphorus removal reactor. Appl. Environ. Microbiol. 65:1251-1258.
45. Odham, G., A. Tunlid, G. Westerdahl, and P. Mårdén. 1986. Combined determination of poly-ß-hydroxyalkanoic and cellular fatty acids in starved marine bacteria and sewage sludge by gas chromatography with flame ionization or mass spectrometry detection. Appl. Environ. Microbiol. 52:905-910.
46. Okabe, S., M. Oshiki, Y. Kamagata, et al. 2010. A great leap forward in microbial ecology. Microbes Environ. 25:230-240.
47. Oshiki, M., M. Onuki, H. Satoh, and T. Mino. 2008. PHAaccumulating microorganisms in full-scale wastewater treatment plants. Water Sci. Technol. 58:13-20.
48. Oshiki, M., M. Onuki, H. Satoh, and T. Mino. 2009. Temporal carbon storage in activated sludge during the removal of organic pollutants in fully aerobic wastewater treatment plants. J. Japan Sewage Works Association. 46:126-137.
49. Oshiki, M., H. Satoh, and T. Mino. 2011. Acetate uptake by PHAaccumulating and non-PHA-accumulating organisms in activated sludge from an aerobic sequencing batch reactor fed with acetate. Water Sci. Technol. 62:8-14.
50. Ostle, A.G., and J.G. Holt. 1982. Nile blue A as a fluorescent stain for poly-ß-hydroxybutyrate. Appl. Environ. Microbiol. 44:238-241.
51. Raunkjær, K., and P.H. Nielsen, T. Hvitved-jacobsen. 1995. Transformation of organic matter in a gravity sewer. Water Environ. Res. 67:181-188.
52. Roller, C., M. Wagner, R. Amann, W. Ludwig, and K.H. Schleifer. 1994. In situ probing of gram-positive bacetria with high DNA G+C content using 23S rRNA-targeted oligonucleotides. Microbiology 140:2849-2858.
53. Rothermich, M.M., R. Guerrero, R.W. Lenz, and A.S. Goodwin. 2000. Characterization, seasonal occurrence, and diel fluctuation of poly(hydroxyalkanoate) in photosynthetic microbial mats. Appl. Environ. Microbiol. 66:4279-4291.
54. Saikaly, P.E., P.G. Stroot, and D.B. Oerther. 2005. Use of 16S rRNA gene terminal restriction fragment analysis to assess the impact of solids retention time on the bacterial diversity of activated sludge. Appl. Environ. Microbiol. 71:5814-5822.
55. Schloss, P.D., S.L. Westcott, T. Ryabin, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
56. Serafim, L.S., P.C. Lemos, C. Levantesi, V. Tandoi, H. Santos, and M.A.M. Reis. 2002. Methods for detection and visualization of intracellular polymers stored by polyphosphate-accumulating microorganisms. J. Microbiol. Methods 51:1-18.
57. Serafim, L.S., P.C. Lemos, S. Rossetti, C. Levantesi, V. Tandoi, and M.A.M. Reis. 2006. Microbial community analysis with a high PHA storage capacity. Water Sci. Technol. 54:183-188.
58. Seviour, R.J., T. Mino, and M. Onuki. 2003. The microbiology of biological phosphorus removal in activated sludge systems. FEMS Microbiol. Reviews 27:99-127.
59. Takabatake, H., H. Satoh, T. Mino, and T. Matsuo. 2002. PHA (polyhydroxyalkanoate) production potential of activated sludge treating wastewater. Water Sci. Technol. 45:119-126.
60. van Gemerden, H., E. Montesinos, J. Mas, and R. Guerrero. 1985. Diel cycle of metabolism of phototrophic purple sulfur bacteria in lake Cisó (Spain). Limnol. Oceanogr. 30:932-943.
61. Vishnuvardhan Reddy, S., M. Thirumala, T.V. Kishore Reddy, and S.K. Mahmood. 2008. Isolation of bacteria producing polyhydroxyalkanoates (PHA) from municipal sewage sludge. World J. Microbiol. Biotechnol. 24:2949-2955.
62. Wagner, M., and A. Loy. 2002. Bacterial community composition and function in sewage treatment systems. Curr. Opin. Biotechnol. 13:218-227.
63. Wallen, L.L., and W.K. Rohwedder. 1974. Poly-ß-hydroxyalkanoate from activated sludge. Environ. Sci. Technol. 8:576-579.
64. Wong, M.T., F.M. Tan, W.J. Ng, and W.T. Liu. 2004. Identification and occurrence of tetrad-forming Alphaproteobacteria in anaerobicaerobic activated sludge processes. Microbiology 150:3741-3748.