Haloacetic acid-degrading bacterial communities in drinking water systems as determined by cultivation and by terminal restriction fragment length polymorphism of PCR-amplified haloacid dehalogenase gene fragments

Journal of Applied Microbiology

Volumn 112, Issue 4, 2012, Pages 809-822

  Grigorescu, A S ^a   Hozalski, R M ^a   Lapara, T M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Afipia; Biodegradation; Drinking water; Haloacetic acids; TRFLP

Indexed keywords

ACTIVATED CARBON; BACTERIA; BIODEGRADATION; CLONING; GENES; WATER DISTRIBUTION SYSTEMS;

AFIPIUM; BACTERIAL COMMUNITY; DEGRADING BACTERIA; DRINKING WATER SAMPLES; DRINKING WATER SYSTEMS; GENE FRAGMENTS; HALOACETIC ACIDS; NOVEL APPLICATIONS; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS; TRFLP;

POTABLE WATER;

BACTERIAL PROTEIN; DEHI PROTEIN; DEHII PROTEIN; DRINKING WATER; HALOACID; UNCLASSIFIED DRUG;

BACTERIUM; BIODEGRADATION; BIOFILM; CARBOXYLIC ACID; DRINKING WATER; FILTER; GENE EXPRESSION; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION;

ACHROMOBACTER; AFIPIA; ARTICLE; BACTERIUM; BACTERIUM CULTURE; BACTERIUM ISOLATION; BIODEGRADATION; BURKHOLDERIA; CONTROLLED STUDY; GENE AMPLIFICATION; HALOACETIC ACID DEGRADING BACTERIUM; MICROBIAL COMMUNITY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PSEUDOMONAS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RHIZOBIUM; WATER SAMPLING; XANTHOBACTER;

BUCHAREST [ROMANIA]; MINNEAPOLIS; MINNESOTA; ROMANIA; SAINT PAUL; UNITED STATES;

AFIPIA; BACTERIA (MICROORGANISMS);

EID: 84858283380     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2012.05239.x     Document Type: Article

References (54)

1. Barth, P.T., Bolton, L. and Thomson, J.C. (1992) Cloning and partial sequencing of an operon encoding two Pseudomonas putida haloalkanoate dehalogenases of opposite stereospecificity. J Bacteriol 174, 2612-2619.
2. Blackwood, C.B., Marsh, T., Kim, S.H. and Paul, E.A. (2003) Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities. Appl Environ Microbiol 69, 926-932.
3. Brokamp, A.A., Happe, B. and Schmidt, F.R.J. (1997) Cloning and nucleotide sequence of a D, L-haloalkanoic acid dehalogenase encoding gene from Alcaligenes xylosoxidans spp. denitrificans ABIV. Biodegradation 7, 283-396.
4. Bruce, K.D. (1997) Analysis of mer gene subclasses within bacterial communities in soils and sediments resolved by fluorescent-PCR-restriction fragment length polymorphism profiling. Appl Environ Microbiol 63, 4914-4919.
5. Cairns, S.S., Cornish, A. and Cooper, R.A. (1996) Cloning, sequencing and expression in Escherichia coli of two Rhizobium sp. genes encoding haloalkanoate dehalogenases of opposite stereospecificity. Eur J Biochem 235, 744-749.
6. Chen, W.J. and Weisel, C.P. (1988) Halogenated DBP concentrations in a distribution system. J Am Water Works Assoc 90, 151-163.
7. Dunbar, J., White, S. and Forney, L. (1997) Genetic diversity through the looking glass: effect of enrichment bias. Appl Environ Microbiol 63, 1326-1331.
8. Edwards, U., Rogall, T., Blöcker, H., Emde, M. and Böttger, E.C. (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17, 7843-7851.
9. Ellis, D.A., Hanson, M.L., Sibley, P.K., Shahid, T., Fineberg, N.A., Solomon, K.R., Muir, D.C.G. and Mabury, S.A. (2001) The fate and persistence of trifluoroacetic and chloroacetic acids in pond waters. Chemosphere 42, 309-318.
10. Green, S.J., Prakash, O., Gihring, T.M., Akob, D.M., Jasrotia, P., Jardine, P.M., Watson, D.B., Brown, S.D. et al. (2010) Denitrifying bacteria isolated from terrestrial subsurface sediments exposed to mixed-waste contamination. Appl Environ Microbiol 76, 3244-3254.
11. Hashimoto, S., Azuma, T. and Otsuki, A. (1998) Distribution, sources, and stability of haloacetic acids in Tokyo Bay, Japan. Environ Toxicol Chem 17, 798-805.
12. Hill, K.E., Marchesi, J.R. and Weightman, A.J. (1999) Investigation of two evolutionarily unrelated halocarboxylic acid dehalogenase gene families. J Bacteriol 181, 2535-2547.
13. Horz, H.P., Rotthauwe, J.H., Lukow, T. and Liesack, W. (2000) Identification of major subgroups of ammonia-oxidizing bacteria in environmental samples by T-RFLP analysis of amoA PCR products. J Microbiol Methods 39, 197-204.
14. Hozalski, R.M., Zhang, L. and Arnold, W.A. (2001) Reduction of haloacetic acids by Fe-0: implications for treatment and fate. Environ Sci Technol 35, 2258-2263.
15. Jones, D.H., Barth, P.T., Byrom, D. and Thomas, C.M. (1992) Nucleotide sequence of the structural gene encoding a 2-haloalkanoic acid dehalogenase of Pseudomonas putida strain AJ1 and purification of the encoded protein. J Gen Microbiol 138, 675-683.
16. Kawasaki, H., Tsuda, K., Matsushita, I. and Tonomura, K. (1992) Lack of homology between two haloacetate dehalogenase genes encoded on a plasmid from Moraxella sp. strain B. J Gen Microbiol 138, 1317-1323.
17. Kawasaki, H., Toyama, T., Maeda, T., Nishino, H. and Tonomura, K. (1994) Cloning and sequence analysis of a plasmid-encoded 2-haloacid dehalogenase gene from Pseudomonas putida no. 109. Biosci Biotechnol Biochem 58, 160-163.
18. Kerr, L.M. and Marchesi, J.R. (2006) Isolation of novel bacteria able to degrade alpha-halocarboxylic acids by enrichment from environmental samples. Chemosphere 64, 848-855.
19. Krasner, S.W., Weinberg, H.S., Richardson, D.S., Pastor, S.J., Chinn, R., Sclimenti, M.J., Onstad, G.D. and Thruston, A.D. (2006) Occurrence of a new generation of disinfection byproducts. Environ Sci Technol 40, 7175-7185.
20. Kurihara, T., Liu, J.-Q., Nardi-Dei, V., Koshikawa, H., Esaki, N. and Soda, K. (1995) Comprehensive site-directed mutagenesis of L-2-haloacid dehalogenase to probe catalytic amino acid residues. J Biochem 117, 1317-1322.
21. Leach, L.H., Zhang, P., LaPara, T.M., Hozalski, R.M. and Camper, A.K. (2009) Detection and enumeration of haloacetic acid-degrading bacteria in drinking water distribution systems using dehalogenase genes. J Appl Microbiol 107, 978-988.
22. Lebel, G.L., Benoit, F.M. and Williams, D.T. (1997) A one-year survey of halogenated disinfection by-products in the distribution system of treatment plants using three different disinfection processes. Chemosphere 34, 2301-2317.
23. Li, F., Hullar, M.A. and Lampe, J.W. (2007) Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J Microbiol Methods 68, 303-311.
24. Liu, J.Q., Kurihara, T., Hasan, A.K., Nardi-Dei, V., Koshikawa, H., N. Esaki, N. and Soda, K. (1994) Purification and characterization of thermostable and nonthermostable 2-haloacid dehalogenases with different stereospecificities from Pseudomonas sp. strain YL. Appl Environ Microbiol 60, 2389-2393.
25. Mangiapan, S., Benfenati, E., Grasso, P., Terreni, M., Pregnolato, M., Pagani, G. and Barcelo, D. (1997) Metabolites of alachlor in water: identification by mass spectrometry and chemical synthesis. Environ Sci Technol 31, 3637-3646.
26. Marchesi, J.R. and Weightman, A.J. (2003) Comparing the dehalogenase gene pool in cultivated alpha-halocarboxylic acid-degrading bacteria with the environmental metagene pool. Appl Environ Microbiol 69, 4375-4382.
27. McRae, B.M., LaPara, T.M. and Hozalski, R.M. (2004) Biodegradation of haloacetic acids by bacterial enrichment cultures. Chemosphere 55, 915-925.
28. Motosugi, K., Esaki, N. and Soda, K. (1982) Purification and properties of a new enzyme, DL-2-haloacid dehalogenase, from Pseudomonas sp. J Bacteriol 150, 522-527.
29. Murdiyatmo, U., Asmara, W., Tsang, J.S., Baines, A.J., Bull, A.T. and Hardman, D.J. (1992) Molecular biology of the 2-haloacid halidohydrolase IVa from Pseudomonas cepacia MBA4. Biochem J 284, 87-93.
30. Muyzer, G., Teske, A., Wirsen, C.O. and Jannasch, H.W. (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164, 165-172.
31. Nardi-Dei, V., Kurihara, T., Park, C., Esaki, N. and Soda, K. (1997) Bacterial DL-2-haloacid dehalogenase from Pseudomonas sp. 113: gene cloning and structural comparison with D- and L-2-haloacid dehalogenases. J Bacteriol 179, 4232-4238.
32. Noda, S., Ohkuma, M., Usami, R., Horikoshi, K. and Kudo, T. (1999) Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis. Appl Environ Microbiol 65, 4935-4942.
33. Olaniran, A.O., Babalola, G.O. and Okoh, A.I. (2001) Aerobic dehalogenation potentials of four bacterial species isolated from soil and sewage sludge. Chemosphere 45, 45-50.
34. Pals, J.A., Ang, J.K., Wagner, E.D. and Plewa, M.J. (2011) Biological mechanism for the toxicity of haloacetic acid drinking water disinfection byproducts. Environ Sci Technol 45, 5791-5797.
35. Plewa, M.J., Simmons, J.E., Richardson, S.D. and Wagner, E.D. (2010) Mammalian cell cytotoxicity and genotoxicity of the haloacetic acids, a major class of drinking water disinfection by-products. Environ Mol Mutagen 51, 871-878.
36. van der Ploeg, J., Vanhall, G. and Janssen, D.B. (1991) Characterization of the haloacid dehalogenase from Xanthobacter autotrophicus GJ10 and sequencing of the dhlB gene. J Bacteriol 173, 7925-7933.
37. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
38. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
39. Sanchez, J.I., Rossetti, L., Martinez, B., Rodriguez, A. and Giraffa, G. (2006) Application of reverse transcriptase PCR-based T-RFLP to perform semi-quantitative analysis of metabolically active bacteria in dairy fermentations. J Microbiol Methods 65, 268-277.
40. Singer, P.C. (1994) Control of disinfection by-products in drinking water. J Environ Eng 120, 727-744.
41. Singer, P.C., Obolensky, A. and Greiner, A. (1995) DBPs in chlorinated North Carolina drinking waters. J Am Water Works Assoc 87, 83-92.
42. Speight, V.L. and Singer, P.C. (2005) Association between residual chlorine and reduction in haloacetic acid concentrations in distribution systems. J Am Water Works Assoc 97, 82-91.
43. Stringfellow, J.M., Cairns, S.S., Cornish, A. and Cooper, R.A. (1997) Haloalkanoate dehalogenase II (DehE) of a Rhizobium sp. - molecular analysis of the gene and formation of carbon monoxide from trihaloacetate by the enzyme. Eur J Biochem 250, 789-793.
44. Sung, W., Reilley-Matthews, B., O'Day, D.K. and Horrigan, K. (2000) Modeling DBP formation. J Am Water Works Assoc 92, 53-63.
45. Thomas, A.W., Topping, A.W., Slater, J.H. and Weightman, A.J. (1992) Localization and functional analysis of structural and regulatory dehalogenase genes carried on DEH from Pseudomonas putida PP3. J Bacteriol 174, 1941-1947.
46. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
47. USEPA (1998) National Primary Drinking Water Regulations: Disinfectants and Disinfection Byproducts. Final Rule. EPA 815-F-98-010. Washington, DC: US Environmental Protection Agency.
48. USEPA (2006) Stage two disinfection byproduct rule. [Pamphlet].
49. Wilson, R.I. and Mabury, S.A. (2000) Photodegradation of metolachlor: isolation, identification, and quantification of monochloroacetic acid. J Agric Food Chem 48, 944-950.
50. Xie, Y.F. and Zhou, H. (2002) Use of BAC for HAA removal, part 2: column study. J Am Water Works Assoc 94, 126-134.
51. Zhang, X.R. and Minear, R.A. (2002) Decomposition of trihaloacetic acids and formation of the corresponding trihalomethanes in drinking water. Water Res 36, 3665-3673.
52. Zhang, L., Arnold, W.A. and Hozalski, R.M. (2004) Kinetics of haloacetic acid reactions with Fe(0). Environ Sci Technol 38, 6881-6889.
53. Zhang, P., Hozalski, R.M., Leach, L.H., Camper, A.K., Goslan, E.H., Parsons, S.A., Xie, Y.F. and LaPara, T.M. (2009a) Isolation and characterization of haloacetic acid-degrading Afipia spp. from drinking water. FEMS Microbiol Lett 297, 203-208.
54. Zhang, P., LaPara, T.M., Goslan, E.H., Xie, Y., Parsons, S.A. and Hozalski, R.M. (2009b) Biodegradation of haloacetic acids by bacterial isolates and enrichment cultures from drinking water systems. Environ Sci Technol 43, 3169-3175.