Single-cell protein profiling of wastewater enterobacterial communities predicts disinfection efficiency

Applied and Environmental Microbiology

Volumn 69, Issue 7, 2003, Pages 4227-4235

  Ponniah, Gomathinayagam ^a   Chen, Han ^a   Michielutti, Ronda ^a   Salonen, Nancy ^a   Blum, Paul ^a,b  

^a UNIVERSITY OF NEBRASKA   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELLS; FLUORESCENCE; PROTEINS; WASTEWATER TREATMENT;

SINGLE-CELL PROTEINS;

MICROBIOLOGY;

BACTERIAL PROTEIN; CELL PROTEIN; DPS PROTEIN; FACTOR FOR INVERSION STIMULATION; POLYCLONAL ANTIBODY; UNCLASSIFIED DRUG;

BACTERIUM; DISINFECTION; MICROORGANISM; WASTEWATER TREATMENT;

ARTICLE; BACTERIAL FLORA; BACTERIUM CONTAMINATION; DISINFECTION; ENTEROBACTERIACEAE; EPIFLUORESCENCE MICROSCOPE; NONHUMAN; PROTEIN ANALYSIS; TRICKLING FILTER; WASTE WATER; WASTE WATER MANAGEMENT;

BACTERIAL PROTEINS; DISINFECTION; DNA-BINDING PROTEINS; ENTEROBACTERIACEAE; FACTOR FOR INVERSION STIMULATION PROTEIN; FILTRATION; HEAT; SEWAGE; WASTE DISPOSAL, FLUID; WATER MICROBIOLOGY; WATER PURIFICATION; WATER SUPPLY;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; NEGIBACTERIA;

EID: 0037816368     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.7.4227-4235.2003     Document Type: Article

References (54)

1. Almiron, M., A. J. Link, D. Furlong, and R. Kolter. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:2646-2654.
2. Azam, T. A., A. Iwata, A. Nishimura, S. Ueda, and A. Ishihama. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181:6361-6370.
3. Ball, C. A., R. Osuna, K. C. Ferguson, and R. C. Johnson. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. Nebraska, Lincoln, NE J. Bacteriol. 174:8043-8056.
4. Berg, J. D., A. Matin, and P. V. Roberts. 1982. Effects of antecedent growth conditions on sensitivity of Escherichia coli to chlorine dioxide. Appl. Environ. Microbiol. 44:814-819.
5. Chauret, P. C., C. Z. Radziminski, M. Lepuil, R. Creason, and R. C. Andrews. 2001. Chlorine dioxide inactivation of Cryptosporidium parvum oocysts and bacterial spore indicators. Appl. Environ. Microbiol. 67:2993-3001.
6. De los Reyes, F. L., W. Ritter, and L. Raskin. 1997. Group-specific small-subunit rRNA hybridization probes to characterize filamentous foaming in activated sludge systems. Appl. Environ. Microbiol. 63:1107-1117.
7. De los Reyes, M. F., F. de los Reyes, L. Hernandez, and L. Rakin. 1998. Quantification of Gordonia amarae strains in foaming activated sludge and anaerobic digester systems using oligonucleotide hybridization probes. Appl. Environ. Microbiol. 64:2503-2512.
8. De los Reyes, M. F., D. B. Oerther, F. de los Reyes, L. Hernandez, and L. Rakin. 1998. Characterization of filamentous foaming in activated sludge systems using oligonucleotide hybridization and antibody probes. Water Sci. Technol. 37:485-493.
9. Dukan, S., and D. Touati. 1996. Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress. J. Bacteriol. 178:6145-6150.
10. Eaten, A. D., L. S. Clesceri, and A. E. Greenberg (ed.). 1995. Standard methods for the examination of water and wastewater, 19th ed. American Public Health Association, Washington, D.C.
11. Erhart, R., D. Bradford, R. Seviour, R. Amann, and L. Blackall. 1997. Development and use of fluorescent in situ hybridization probes for the detection and identification of Microthrix parvicella in activated sludge. Syst. Appl. Microbiol. 20:310-318.
12. Giovannoni, S. J., E. F. DeLong, G. J. Olsen, and N. R. Pace. 1988. Phylogenetic group specific oligodeoxynucleotide probes for identification of single microbial cells. J. Bacteriol. 170:720-726.
13. Howgrave-Grahan, A. R., and P. L. Steyn. 1988. Application of the fluorescent-antibody technique for the detection of Sphaerotilus nalans in activated sludge. Appl. Environ. Microbiol. 54:799-802.
14. Johnson, R. C., C. A. Ball, D. Pfeffer, and M. I. Simon. 1988. Isolation of the gene encoding the Hin recombinational enhancer binding protein. Proc. Natl. Acad. Sci. USA 85:3484-3488.
15. Kappeler, J., and W. Gujer. 1992. Estimation of kinetic parameters of heterotrophic biomass under aerobic conditions and characterization of wastewater for activated sludge modeling. Water Sci. Technol. 25:125-139.
16. Koch, C., J. Vandekerekhove, and R. Kahmann. 1988. Escherichia coli host factor for site-specific DNA inversion: cloning and characterization of the fis gene. Proc. Natl. Acad. Sci. USA 85:4237-4241.
17. Krska, J., T. Elthon, and P. Blum. 1993. Monocolonal antibody recognition and functions of a DnaK (HSP70) epitope found in gram-negative bacteria. J. Bacteriol. 175:6433-6440.
18. LeChevallier, M. W., C. D. Cawthon, and R. G. Lee. 1988. Factors promoting survival of bacteria in chlorinated water supplies. Appl. Environ. Microbiol. 54:649-654.
19. Lisle, J. H., S. C. Broadaway, A. M. Prescott, B. H. Pyle, C. Fricker and G. A. McFeters. 1998. Effects of starvation on physiological activity and chlorine disinfection resistance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 64:4658-4662.
20. 38-dependent expression of a core Escherichia coli starvation gene, pexB. J. Bacteriol. 176:3928-3935.
21. Manz, W., R. Amann, W. Ludwig, M. Wagner, and K. H. Schleifer. 1992. Phylogenetic oligooxynuleotide probes for the major subclass of Proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15:593-600.
22. Manz, W., U. Szewzyk, P. Ericsson, R. Amaan, K. H. Schleifer, and T. A. Stenstrom. 1993. In situ identification of bacteria in drinking water and adjoining biofilms by hybridization with 16S and 23S rRNA-directed fluorescent oligonucleotide probes. Appl. Environ. Microbiol. 59:2293-2298.
23. Mason, C., and T. Egli. 1993. Dynamics of microbial growth in the decelerating and stationary phase of batch culture, p. 81-102. In S. Kjelleber (ed.), Starvation in bacteria. Plenum Press, New York, N.Y.
24. Matin, A. 1991. The molecular basis of carbon-starvation- induced general resistance in Escherichia coli. Mol. Microbiol. 5:3-10.
25. Matin, A., and S. Harakeh. 1990. Effect of starvation on bacterial resistance to disinfectants, p. 88-103. In G. A. McFeters (ed.), Drinking water microbiology. Springer-Verlag, New York, N.Y.
26. Mittleman, M. W., M. Habash, J. M. Lacroix, A. E. Khoury, and M. Krajden. 1997. Rapid detection of Enterobacteriaceae in urine by fluorescent 16S rRNA in situ hybridization on membrane filters. J. Microbiol. Methods 30:153-160.
27. Nilsson, L., H. Verbeek, E. Vijgenboom, C. van Drunen, A. Vanet, and L. Bosch. 1992. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J. Bacteriol. 174:921-929.
28. Notley, L., and T. Ferenci. 1996. Induction of RpoS-dependent functions in glucose-limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli? J. Bacteriol. 178:1465-1468.
29. Oerther, D. B., F. L. de los Reyes, and L. R Askin. 1999. Interfacing phylogenetic oligonucleotide probe hybridization with representations of microbial populations and specific growth rates in mathematical models of activated sludge process. Water. Sci. Technol. 39:11-20.
30. Ogoshi, M., Y. Suzuki, and T. Asano. 2001. Water reuse in Japan. Water Sci. Technol. 43:17-23.
31. Olsen, B., and M. Stewart. 1987. Factors that change bacterial resistance to disinfection, p. 885-904. In R. L. Jolley, L. W. Condie, J. D Johnson, S. Katz, R. A. Minear, J. S. Mattice, and V. A Jacobs (ed.), Water chlorination: chemistry, environmental impact and health effects, vol. 6. Lewis Publishers, Inc., Chelsea, Mich.
32. Olsen, G. J., D. J. Lane, S. J. Giovannoni, N. R. Pace, and D. A. Stahl. 1986. Microbial ecology and evolution; a ribosomal RNA approach. Annu. Rev. Microbiol. 40:337-365.
33. Onuki, M., H. Satoh, and T. Mino. 2002. Analysis of microbial community that performs enhanced biological phosphorus removal in activated sludge fed with acetate. Water Sci. Technol. 46:145-154.
34. Porter, K. G., and Y. S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25:943-948.
35. Poulsen, L. K., G. Ballard, and D. A. Stahl. 1993. Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms. Appl. Environ. Microbiol. 59:1354-1360.
36. Preez, M., R. Kfir, and P. Coubrough. 1995. Investigation of injury of enterobacteria after chlorination. Water Sci. Technol. 31:115-118.
37. Rittman, B. E., and P. L. McCarty (ed.). 2001. Environmental biotechnology: principles and applications. McGraw-Hill Higher Education. New York, N.Y.
38. 2 resistance, and reductive division. J. Bacteriol. 177: 3695-3703.
39. Rockabrand, D., K. Livers, T. Austin, R. Kaiser, D. Jensen, R. Burgess, and P. Blum. 1998. Roles of DnaK and RpoS in starvation-induced thermotolerance of Escherichia coli. J. Bacteriol. 180:846-854.
40. Rockabrand, D., T. Austin, R. Kaiser, and P. Blum. 1999. Bacterial growth state distinguished by single-cell protein profiling: does chlorination kill coliforms in municipal effluent? Appl. Environ. Microbiol. 65:4181-4188.
41. Schuppler, M., M. Wagner., G. Schon, and U. B. Gobel. 1998. In situ hybridization of nocardioforms in activated sludge using fluorescent rRNA targeted oligonucleotide probes. Microbiology 144:249-259.
42. Standridge, J. H., and J. J. Delfino. 1981. A-1 medium: alternative technique for fecal coliform organism enumeration in chlorinated wastewaters. Appl. Environ. Microbiol. 42:918-920.
43. Stewart, M., and B. Olson. 1992. Physiological studies of chloramine resistance developed by Klebsiella pneumoniae to chloramines. Appl. Environ. Microbiol. 58:2649-2653.
44. Szewzyk, U., W. Manz, R. Amaan, K. H. Schleifer, and T. A. Stenstrom. 1994. Growth and in situ detection of a pathogenic Escherichia coli in biofilms of a heterotrophic water-bacterium by use of 16S and 23S rRNA-directed fluorescent oligonucleotide probes. FEMS Microbiol. Ecol. 13:169-176.
45. Thompson, J. F., L. Moitoso de Vargas, D. Kock, R. Kahmann, and A. Landy. 1987. Cellular factors couple recombinations with growth phase: characterization of a new component in the λ site-specific recombination pathway. Cell 50:901-908.
46. U.S. Environmental Protection Agency. 1995. National pollutant discharge elimination system permit application requirements for publicly owned treatment works and other treatment works treating domestic sewage. Fed. Regist. 60:62562-62569.
47. Villanueva, C., M. Kogevinas, and J. Grimalt. 2001. Chlorination of drinking water in Spain and bladder cancer. Gac. Sanit. 15:48-53.
48. Volsch, A., W. F. Nader, H. K. Geiss, G. Nebe, and C. Birr. 1990. Detection and analysis of two serotypes of ammonia-oxidizing bacteria in sewage plants by flow cytometry. Appl. Environ. Microbiol. 56:2430-2435.
49. Wagner, M., R. Amann, H. Lemmer, and K. H. Schleifer. 1993. Probing activated sludge with oligonucleotides specific for proteobacteria: inadequacy of culture-dependent methods for describing microbial community structure. Appl. Environ. Microbiol. 59:1520-1525.
50. Wagner, M., R. Amaan, H. Lemmer, W. Manz, and K. H. Schleifer. 1994. Probing activated sludge with fluorescently labeled rRNA targeted oligonucleotides. Water Sci. Technol. 29:15-23.
51. Wagner, M., R. Erhart, W. Manz, R. Amann, H. Lemmer., D. Wedi, and K. H. Schleifer. 1994. Development of an rRNA targeted oligonucleotide probe specific for the genus Acinetobacter and its application for in situ monitoring in activated sludge. Appl. Environ. Microbiol. 60:792-800.
52. Wintzingercode, F. V., U. B. Gobel, and E. Stackebrabdt. 1997. Determination of microbial diversity in environmental samples: pitfalls of PCR based rRNA analysis. FEMS Microbiol. Rev. 21:213-229.
53. Xu, P., F. Brissaud, J. C. Maihol, F. Valette, and V. Lazarova. 2002. Design of climate-dependent water reuse project. Water Sci. Technol. 46:289-296.
54. Zarda, B., R. Amann, G. Wallner, and K. H. Schliefer. 1991. Identification of single bacterial cells using digoxigenin-labelled rRNA-targeted oligonucleotides. J. Gen. Microbiol. 137:2823-2830.