Identification and environmental distribution of dcpA, which encodes the reductive dehalogenase catalyzing the dichloroelimination of 1,2-dichloropropane to propene in organohalide-respiring Chloroflexi

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 808-818

  Padilla Crespo, Elizabeth ^a,b   Yan, Jun ^a,b   Swift, Cynthia ^a,b   Wagner, Darlene D ^c   Chourey, Karuna ^b   Hettich, Robert L ^b   Ritalahti, Kirsti M ^a,b   Löffler, Frank E ^a,b,d  

^a UNIVERSITY OF TENNESSEE   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d University of Tennessee Knoxville   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ,2-DICHLOROPROPANE; ELECTRON ACCEPTOR; ENRICHMENT CULTURE; ENVIRONMENTAL DISTRIBUTION; GEOGRAPHICAL LOCATIONS; INORGANIC CHLORIDE; QUANTITATIVE REAL TIME PCR; REDUCTIVE DEHALOGENASES;

BIOREMEDIATION; CHLORINE COMPOUNDS; GENES; POLYMERASE CHAIN REACTION; STRAIN; TRANSCRIPTION;

PROPYLENE;

ALKENE; BACTERIUM; BIOREMEDIATION; CATALYSIS; CHLORINATED HYDROCARBON; ENZYME ACTIVITY; FLUVIAL DEPOSIT; GENE EXPRESSION; LAND RECLAMATION; MICROCOSM; ORGANOHALOGEN; POLYMERASE CHAIN REACTION;

ALKENE; BACTERIAL DNA; DRUG DERIVATIVE; HYDROLASE; PROPANE; PROPYLENE; PROPYLENE DICHLORIDE;

ARTICLE; CHEMISTRY; CHLOROFLEXI; CLUSTER ANALYSIS; DNA SEQUENCE; ENZYMOLOGY; EUROPE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SOUTH AMERICA;

ALKENES; CHLOROFLEXI; CLUSTER ANALYSIS; DNA, BACTERIAL; EUROPE; GENE EXPRESSION PROFILING; HYDROLASES; MOLECULAR SEQUENCE DATA; NORTH AMERICA; PHYLOGENY; PROPANE; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA; WATER MICROBIOLOGY;

EID: 84892951187     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02927-13     Document Type: Article

References (61)

1. Agency for Toxic Substances and Disease Registry (ATSDR). 1989. Toxicological profile for 1,2-dichloropropane. U.S. Department of Health and Human Services, Public Health Service, Atlanta, GA.
2. Nijhuis TA, Makkee M, Moulijn JA, Weckhuysen BM. 2006. The production of propene oxide: catalytic processes and recent developments. Ind. Eng. Chem. Res. 45:3447-3459. http://dx.doi.org/10.1021/ie0513090.
3. Zogorski JS, Carter JM, Ivahnenko T, Lapham WW, Moran MJ, Rowe BL, Squillace PJ, Toccalino PL. 2006. Volatile organic compounds in the nation's ground water and drinking-water supply wells. U.S. Geol. Surv. Circ. 129:101.
4. Pacific Biomedical Research Center. 1975. Hawaii epidemiologic studies program annual report no. 8, p 176. University of Hawaii, Honolulu, HI.
5. Schlötelburg C, von Wintzingerode C, Hauck R, von Wintzingerode F, Hegemann W, Göbel UB. 2002. Microbial structure of an anaerobic bioreactor population that continuously dechlorinates 1,2-D. FEMS Microbiol. Ecol. 39:229-237. http://dx.doi.org/10.1111/j.1574-6941.2002.tb00925.x.
6. De Wildeman S, Diekert G, Van Langenhove H, Verstraete W. 2003. Stereoselective microbial dehalorespiration with vicinal dichlorinated alkanes. Appl. Environ. Microbiol. 69:5643-5647. http://dx.doi.org/10.1128 /AEM.69.9.5643-5647.2003.
7. Moe WM, Yan J, Nobre MF, da Costa MS, Rainey FA. 2009. Dehalogenimonas lykanthroporepellens gen. nov., sp. nov., a reductively dehalogenating bacterium isolated from chlorinated solvent-contaminated groundwater. Int. J. Syst. Evol. Microbiol. 59:2692-2697. http://dx.doi .org/10.1099/ijs.0.011502-0.
8. Bowman KS, Nobre MF, da Costa MS, Rainey FA, Moe WM. 2013. Dehalogenimonas alkenigignens sp. nov., a chlorinated-alkanedehalogenating bacterium isolated from groundwater. Int. J. Syst. Evol. Microbiol. 63:1492-1498. http://dx.doi.org/10.1099/ijs.0.045054-0.
9. Löffler FE, Champine JE, Ritalahti KM, Sprague SJ, Tiedje JM. 1997. Complete reductive dechlorination of 1,2-dichloropropane by anaerobic bacteria. Appl. Environ. Microbiol. 63:2870-2875.
10. Ritalahti KM, Löffler FE. 2004. Populations implicated in the anaerobic reductive dechlorination of 1,2-dichloropropane in highly enriched bacterial communities. Appl. Environ. Microbiol. 70:4088-4095. http://dx .doi.org/10.1128/AEM.70.7.4088-4095.2004.
11. Löffler FE, Yan J, Ritalahti KM, Adrian L, Edwards EA, Konstantinidis KT, Müller JA, Fullerton H, Zinder SH, Spormann AM. 2013. Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi. Int. J. Syst. Evol. Microbiol. 63:625-635. http://dx.doi .org/10.1099/ijs.0.034926-0.
12. Yan J, Rash BA, Rainey FA, Moe WM. 2009. Isolation of novel bacteria within the Chloroflexi capable of reductive dechlorination of 1,2,3-trichloropropane. Environ. Microbiol. 11:833-843. http://dx.doi.org/10 .1111/j.1462-2920.2008.01804.x.
13. He J, Sung Y, Dollhopf ME, Fathepure BZ, Tiedje JM, Löffler FE. 2002. Acetate versus hydrogen as direct electron donors to stimulate the microbial reductive dechlorination process at chloroethene-contaminated sites. Environ. Sci. Technol. 36:3945-3952. http://dx.doi.org/10.1021/es025528d.
14. Löffler FE, Sanford RA, Tiedje JM. 1996. Initial characterization of a reductive dehalogenase from Desulfitobacterium chlororespirans Co23. Appl. Environ. Microbiol. 62:3809-3813.
15. Wolin EA, Wolin MJ, Wolfe RS. 1963. Formation of methane by bacterial extracts. J. Biol. Chem. 238:2882-2886.
16. Amos BK, Christ JA, Abriola LM, Pennell KD, Löffler FE. 2007. Experimental evaluation and mathematical modeling of microbially enhanced tetrachloroethene (PCE) dissolution. Environ. Sci. Technol. 41:963-970. http://dx.doi.org/10.1021/es061438n.
17. Ritalahti KM, Cruz-García C, Padilla-Crespo E, Hatt JK, Löffler FE. 2010. RNA extraction and cDNA analysis for quantitative assessment of biomarker transcripts in groundwater, p 3671-3685. In Timmis KN (ed), Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Germany.
18. Krajmalnik-Brown R, Hölscher T, Thomson IN, Saunders FM, Ritalahti KM, Löffler FE. 2004. Genetic identification of a putative vinyl chloride reductase in Dehalococcoides sp. strain BAV1. Appl. Environ. Microbiol. 70:6347-6351. http://dx.doi.org/10.1128/AEM.70.10.6347-6351.2004.
19. Hatt JK, Löffler FE. 2012. Quantitative real-time PCR (qPCR) detection chemistries affect enumeration of the Dehalococcoides 16S rRNA gene in groundwater. J. Microbiol. Methods 88:263-270. http://dx.doi.org/10 .1016/j.mimet.2011.12.005.
20. Ritalahti KM, Amos BK, Sung Y, Wu Q, Koenigsberg SS, Löffler FE. 2006. Quantitative PCR targeting 16S rRNA and reductive dehalogenase genes simultaneously monitors multiple Dehalococcoides strains. Appl. Environ. Microbiol. 72:2765-2774. http://dx.doi.org/10.1128/AEM.72.4 .2765-2774.2006.
21. ABI. 2005. Applied Biosystems 7900HT fast real-time PCR system and 7300/7500 real-time PCR systems: chemistry guide 4348358, revision E. ABI, Foster City, CA.
22. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55:611-622. http: //dx.doi.org/10.1373/clinchem.2008.112797.
23. Johnson DR, Lee PK, Holmes VF, Alvarez-Cohen L. 2005. An internal reference technique for accurately quantifying specific mRNAs by realtime PCR with application to the tceA reductive dehalogenase gene. Appl. Environ. Microbiol. 71:3866-3871. http://dx.doi.org/10.1128/AEM.71.7 .3866-3871.2005.
24. Fung JM, Morris RM, Adrian L, Zinder SH. 2007. Expression of reductive dehalogenase genes in Dehalococcoides ethenogenes strain 195 growing on tetrachloroethene, trichloroethene, or 2,3-dichlorophenol. Appl. Environ. Microbiol. 73:4439-4445. http://dx.doi.org/10.1128 /AEM.00215-07.
25. Chow WL, Cheng D, Wang S, He J. 2010. Identification and transcriptional analysis of trans-DCE-producing reductive dehalogenases in Dehalococcoides species. ISME J. 4:1020-1030. http://dx.doi.org/10.1038/ismej .2010.27.
26. Rahm BG, Morris RM, Richardson RE. 2006. Temporal expression of respiratory genes in an enrichment culture containing Dehalococcoides ethenogenes. Appl. Environ. Microbiol. 72:5486-5491. http://dx.doi.org /10.1128/AEM.00855-06.
27. Thompson JD, Higgins DG. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix. Nucleic Acids Res. 22:4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673.
28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
29. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
30. Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York, NY.
31. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791. http://dx.doi.org/10.2307/2408678.
32. Seshadri R, Adrian L, Fouts DE, Eisen JA, Phillippy AM, Methe BA, Ward NL, Nelson WC, Deboy RT, Khouri HM, Kolonay JF, Dodson RJ, Daugherty SC, Brinkac LM, Sullivan SA, Madupu R, Nelson KE, Kang KH, Impraim M, Tran K, Robinson JM, Forberger HA, Fraser CM, Zinder SH, Heidelberg JF. 2005. Genome sequence of the PCEdechlorinating bacterium Dehalococcoides ethenogenes. Science 307:105-108. http://dx.doi.org/10.1126/science.1102226.
33. Tang S, Chan WW, Fletcher KE, Seifert J, Liang X, Löffler FE, Edwards EA, Adrian L. 2013. Functional characterization of reductive dehalogenases by using blue native polyacrylamide gel electrophoresis. Appl. Environ. Microbiol. 79:974-981. http://dx.doi.org/10.1128/AEM.01873-12.
34. Tabb DL, Fernando CG, Chambers MC. 2007. MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6:654-661. http://dx.doi.org/10 .1021/pr0604054.
35. Holman JD, Ma ZQ, Tabb DL. 2012. Identifying proteomic LC-MS/MS data sets with Bumbershoot and IDPicker. Curr. Protoc. Bioinformatics Chapter 13:Unit13.17. http://dx.doi.org/10.1002/0471250953.bi1317s37.
36. Smidt H, van Leest M, van Der Oost J, de Vos WM. 2000. Transcriptional regulation of the cpr gene cluster in ortho-chlorophenol-respiring Desulfitobacterium dehalogenans. J. Bacteriol. 182:5683-5691. http://dx .doi.org/10.1128/JB.182.20.5683-5691.2000.
37. Gábor K, Veríssimo CS, Cyran BC, Ter Horst P, Meijer NP, Smidt H, de Vos WM, van der Oost J. 2006. Characterization of CprK1, a CRP/ FNR-type transcriptional regulator of halorespiration from Desulfitobacterium hafniense. J. Bacteriol. 188:2604-2613. http://dx.doi.org/10.1128 /JB.188.7.2604-2613.2006.
38. Ludwig ML, Matthews RG. 1997. Structure-based perspectives on B12-dependent enzymes. Annu. Rev. Biochem. 66:269-313. http://dx.doi.org /10.1146/annurev.biochem.66.1.269.
39. Hug LA Maphosa F, Leys D, Löffler FE, Smidt H, Edwards EA, Adrian L. 2013. Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368: 20120322. http://dx.doi.org/10.1098/rstb.2012.0322.
40. Reddy P, Peterkofsky A, McKenney K. 1985. Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG initiation codon to GUGorAUGresults in increased gene expression. Proc. Natl. Acad. Sci. U. S. A. 82:5656-5660. http://dx.doi.org/10.1073/pnas.82.17.5656.
41. Dolfing J, Janssen DB. 1994. Estimates of Gibbs free energies of formation of chlorinated aliphatic compounds. Biodegradation 5:21-28.
42. Waller AS, Krajmalnik-Brown R, Löffler FE, Edwards EA. 2005. Multiple reductive-dehalogenase-homologous genes are simultaneously transcribed during dechlorination by Dehalococcoides-containing cultures. Appl. Environ. Microbiol. 71:8257-8264. http://dx.doi.org/10.1128/AEM .71.12.8257-8264.2005.
43. Futamata H, Kaiya S, Sugawara M, Hiraishi A. 2009. Phylogenetic and transcriptional analyses of a tetrachloroethene-dechlorinating "Dehalococcoides" enrichment culture TUT2264 and its reductive-dehalogenase genes. Microbes Environ. 24:330-337. http://dx.doi.org/10.1264/jsme2 .ME09133.
44. Lee PK, Macbeth TW, Sorenson KJS, Deeb RA, Alvarez-Cohen L. 2008. Quantifying genes and transcripts to assess the in situ physiology of "Dehalococcoides" spp. in a trichloroethene-contaminated groundwater site. Appl. Environ. Microbiol. 74:2728-2739. http://dx.doi.org/10.1128/AEM .02199-07.
45. Johnson DR, Brodie EL, Hubbard AE, Andersen GL, Zinder SH, Alvarez-Cohen L. 2008. Temporal transcriptomic microarray analysis of "Dehalococcoides ethenogenes" strain 195 during the transition into stationary phase. Appl. Environ. Microbiol. 74:2864 -2872. http://dx .doi.org/10.1128/AEM.02208-07.
46. Rahm BG, Richardson RE. 2008. Correlation of respiratory gene expression levels and pseudo-steady-state PCE respiration rates in Dehalococcoides ethenogenes. Environ. Sci. Technol. 42:1599. http://dx.doi.org/10 .1021/es071455s.
47. Amos BK, Ritalahti KM, Cruz-Garcia C, Padilla-Crespo E, Löffler FE. 2008. Oxygen effect on Dehalococcoides viability and biomarker quantification. Environ. Sci. Technol. 42:5718-5726. http://dx.doi.org/10.1021 /es703227g.
48. Fletcher KE, Costanza J, Cruz-Garcia C, Ramaswamy NS, Pennell KD, Löffler FE. 2011. Effects of elevated temperature on Dehalococcoides dechlorination performance and DNA and RNA biomarker abundance. Environ. Sci. Technol. 45:712-718. http://dx.doi.org/10.1021/es1023477.
49. Tang S, Edwards EA. 2013. Identification of Dehalobacter reductive dehalogenases that catalyse dechlorination of chloroform, 1,1,1-trichloroethane and 1,1-dichloroethane. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20120318. http://dx.doi.org/10.1098/rstb.2012.0318.
50. Neumann A, Siebert A, Trescher T, Reinhardt S, Wohlfarth G, Diekert G. 2002. Tetrachloroethene reductive dehalogenase of Dehalospirillum multivorans: substrate specificity of the native enzyme and its corrinoid cofactor. Arch. Microbiol. 177:420-426. http://dx.doi.org/10.1007/s00203-002-0409-3.
51. Morris RM, Sowell S, Barofsky D, Zinder S, Richardson R. 2006. Transcription and mass-spectroscopic proteomic studies of electron transport oxidoreductases in Dehalococcoides ethenogenes. Environ. Microbiol. 8:1499-1509. http://dx.doi .org/10.1111/j.1462-2920.2006.01090.x.
52. Morris RM, Fung JM, Rahm BG, Zhang S, Freedman DL, Zinder SH, Richardson RE. 2007. Comparative proteomics of Dehalococcoides spp. reveals strain-specific peptides associated with activity. Appl. Environ. Microbiol. 73:320-326. http://dx.doi.org/10.1128/AEM.02129-06.
53. Furano AV. 1975. Content of elongation factor Tu in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 72:4780-4784. http://dx.doi.org/10.1073 /pnas.72.12.4780.
54. Müller JA, Rosner BM, Von Abendroth G, Meshulam-Simon G, Mc-Carty PL, Spormann AM. 2004. Molecular identification of the catabolic vinyl chloride reductase from Dehalococcoides sp. strain VS and its environmental distribution. Appl. Environ. Microbiol. 70:4880-4888. http: //dx.doi.org/10.1128/AEM.70.8.4880-4888.2004.
55. Krajmalnik-Brown R, Sung Y, Ritalahti KM, Saunders FM, Löffler FE. 2007. Environmental distribution of the trichloroethene reductive dehalogenase gene (tceA) suggests lateral gene transfer among Dehalococcoides. FEMS Microbiol. Ecol. 59:206-214. http://dx.doi.org/10.1111/j.1574 -6941.2006.00243.x.
56. Sung Y, Ritalahti KM, Apkarian RP, Löffler FE. 2006. Quantitative PCR confirms purity of strain GT, a novel trichloroethene (TCE)-to-ethenerespiring Dehalococcoides isolate. Appl. Environ. Microbiol. 72:1980-1987. http://dx.doi.org/10.1128/AEM.72.3.1980-1987.2006.
57. McMurdie PJ, Hug LA, Edwards EA, Holmes S, Spormann AM. 2011. Site-specific mobilization of vinyl chloride respiration islands by a mechanism common in Dehalococcoides. BMC Genomics 12:287. http://dx.doi .org/10.1186/1471-2164-12-287.
58. Duhamel M, Wehr SD, Yu L, Rizvi H, Seepersad D, Dworatzek S, Cox EE, Edwards EA. 2002. Comparison of anaerobic dechlorinating enrichment cultures maintained on tetrachloroethene, trichloroethene, cisdichloroethene and vinyl chloride. Water Res. 36:4193-4202. http://dx .doi.org/10.1016/S0043-1354(02)00151-3.
59. Fletcher KE, Löffler FE, Richnow HH, Nijenhuis I. 2009. Stable carbon isotope fractionation of 1,2-dichloropropane during dichloroelimination by Dehalococcoides populations. Environ. Sci. Technol. 43:6915-6919. http://dx.doi.org/10.1021/es900365x.
60. He J, Ritalahti KM, Aiello MR, Löffler FE. 2003. Complete detoxification of vinyl chloride (VC) by an anaerobic enrichment culture and identification of the reductively dechlorinating population as a Dehalococcoides species. Appl. Environ. Microbiol. 69:996-1003. http://dx.doi.org/10.1128 /AEM.69.2.996-1003.2003.
61. Yan J, Rash BA, Rainey FA, Moe WM. 2009. Detection and quantification of Dehalogenimonas and "Dehalococcoides" populations via PCRbased protocols targeting 16S rRNA genes. Appl. Environ. Microbiol. 75: 7560-7564. http://dx.doi.org/10.1128/AEM.01938-09.