The effect of co-substrate activation on indigenous and bioaugmented PCB dechlorinating bacterial communities in sediment microcosms

Applied Microbiology and Biotechnology

Volumn 89, Issue 6, 2011, Pages 2005-2017

  Park, Joong Wook ^a   Krumins, Valdis ^a   Kjellerup, Birthe V ^b   Fennell, Donna E ^a   Rodenburg, Lisa A ^a   Sowers, Kevin R ^c   Kerkhof, Lee J ^a   Häggblom, Max M ^a  

^a RUTGERS UNIVERSITY   (United States)

^b GOUCHER COLLEGE   (United States)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Dechlorination; Dehalococcoides; Dehalogenation; PCB; rdh genes; Sediments

Indexed keywords

16S RRNA GENE; ANACOSTIA RIVER; BACTERIAL COMMUNITY; BACTERIAL POPULATION; COSUBSTRATES; DEHALOCOCCOIDES; DEHALOCOCCOIDES ETHENOGENES; DEHALOCOCCOIDES SPP; EFFECT OF CO; ENVIRONMENTAL POLLUTANTS; PCB; PHYLOGENETIC ANALYSIS; PHYLOGENETIC APPROACH; RDH GENES; REDUCTIVE DECHLORINATION; REDUCTIVE DEHALOGENASES; SEDIMENT MICROCOSMS; WASHINGTON;

ANOXIC SEDIMENTS; BACTERIOLOGY; DETOXIFICATION; GENES; ORGANIC POLLUTANTS; POLYCHLORINATED BIPHENYLS; RNA; SEDIMENTOLOGY; SUBSTRATES;

DECHLORINATION;

BACTERIAL DNA; BACTERIAL PROTEIN; POLYCHLORINATED BIPHENYL; REDUCTIVE DEHYDROGENASE PROTEIN; RNA 16S; UNCLASSIFIED DRUG;

BACTERIUM; BIOMONITORING; COMMUNITY STRUCTURE; DECHLORINATION; DETOXIFICATION; ENZYME ACTIVITY; FLUVIAL DEPOSIT; GENE EXPRESSION; GENETIC ANALYSIS; MICROCOSM; PCB; PHYLOGENETICS; POLLUTANT; POPULATION STRUCTURE;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BIOREMEDIATION; CHLOROFLEXI; CONTROLLED STUDY; DECHLORINATION; DEHALOCOCCOIDES ETHENOGENES; DENATURING GRADIENT GEL ELECTROPHORESIS; DENATURING HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MICROBIAL COMMUNITY; MICROCOSM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYCHLORINATED BIPHENYL REMOVAL; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEDIMENT; WATER POLLUTANT; WATER POLLUTION CONTROL;

BACTERIA; BIODIVERSITY; CHLORINE; CLUSTER ANALYSIS; DISTRICT OF COLUMBIA; DNA, BACTERIAL; DNA, RIBOSOMAL; ENVIRONMENTAL POLLUTANTS; GEOLOGIC SEDIMENTS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYCHLORINATED BIPHENYLS; RIVERS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

ANACOSTIA RIVER; DISTRICT OF COLUMBIA; UNITED STATES;

ANACOSTIA; BACTERIA (MICROORGANISMS); CHLOROFLEXI; CHLOROFLEXI (CLASS); DEHALOCOCCOIDES; DEHALOCOCCOIDES ETHENOGENES 195;

EID: 79952569355     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-010-2958-8     Document Type: Article

References (64)

1. Adrian L, Szewzyk U, Wecke J, Görisch H (2000) Bacterial dehalorespiration with chlorinated benzenes. Nature 408:580-583
2. Adrian L, Rahnenführer J, Gobom J, Hölscher T (2007) Identification of a chlorobenzene reductive dehalogenase in Dehalococcoides sp. strain CBDB1. Appl Environ Microbiol 73:7717-7724
3. Adrian L, Dudkova V, Demnerova K, Bedard DL (2009) Dehalococcoides sp. strain CBDB1 extensively dechlorinates the commercial polychlorinated biphenyl (PCB) mixture Aroclor 1260. Appl Environ Microbiol 75:4516-4524
4. Ahn YB, Häggblom MM, Fennell DE (2005) Co-amendment with halogenated compounds enhances anaerobic microbial dechlorination of 1,2,3,4- tetrachlorodibenzo-p-dioxin and 1,2,3,4-tetrachlorodibenzofuran in estuarine sediments. Environ Toxicol Chem 24:2775-2784
5. Ahn YB, Häggblom MM, Kerkhof LJ (2007) Comparison of anaerobic microbial communities from estuarine sediments amended with halogenated compounds to enhance dechlorination of 1,2,3,4-tetrachlorodibenzo-p-dioxin. FEMS Microbiol Ecol 61:362-371
6. Ahn YB, Liu F, Fennell DE, Häggblom MM (2008) Biostimulation and bioaugmentation to enhance dechlorination of polychlorinated dibenzo-p-dioxins in contaminated sediments. FEMS Microbiol Ecol 66:271-281
7. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402 (Pubitemid 27359211)
8. 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
9. Bedard DL (2008) A case study for microbial biodegradation: anaerobic bacterial reductive dechlorination of polychlorinated biphenyls - from sediment to defined medium. Annu Rev Microbiol 62:253-270
10. Bedard DL, Quensen JF III (1995) Microbial reductive dechlorination of polychlorinated biphenyls. In: Young LY, Cerniglia C (eds) Microbial transformation and degradation of toxic organic chemicals. Wiley, New York, pp 127-216
11. Bedard DL, Van Dort H, DeWeerd KA (1998) Brominated biphenyls prime extensive microbial reductive dehalogenation of Aroclor 1260 in Housatonic River sediment. Appl Environ Microbiol 64:1786-1795 (Pubitemid 28234785)
12. Bedard DL, Pohl EA, Bailey JJ, Murphy A (2005) Characterization of the PCB substrate range of microbial dechlorination process LP. Environ Sci Technol 39:6831-6838 (Pubitemid 41266170)
13. Bedard DL, Bailey JJ, Reiss BL, Jerzak GV (2006) Development and characterization of stable sediment-free anaerobic bacterial enrichment cultures that dechlorinate Aroclor 1260. Appl Environ Microbiol 72:2460-2470
14. Bedard DL, Ritalahti KM, Löffler FE (2007) The Dehalococcoides population in sediment-free mixed cultures metabolically dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260. Appl Environ Microbiol 73:2513-2521 (Pubitemid 46668743)
15. Behrens S, Azizian MF, McMurdie PJ, Sabalowsky A, Dolan ME, Semprini L, Spormann AM (2008) Monitoring abundance and expression of " Dehalococcoides" species chloroethene-reductive dehalogenases in a tetrachloroethene-dechlorinating flow column. Appl Environ Microbiol 74:5695-5703
16. Carreon-Diazconti C, Santamaria J, Berkompas J, Field JA, Brusseau ML (2009) Assessment of in situ reductive dechlorination using compound-specific stable isotopes, functional gene PCR, and geochemical data. Environ Sci Technol 43:4301-4307
17. Cutter LA, Watts JEM, Sowers KR, May HD (2001) Identification of a microorganism that links its growth to the reductive dechlorination of 2,3,5,6-chlorobiphenyl. Environ Microbiol 3:699-709
18. Duhamel M, Mo K, Edwards EA (2004) Characterization of a highly enriched Dehalococcoides-containing culture that grows on vinyl chloride and trichloroethene. Appl Environ Microbiol 70:5538-5545 (Pubitemid 39279632)
19. Fagervold SK, Watts JE, May HD, Sowers KR (2005) Sequential reductive dechlorination of meta-chlorinated polychlorinated biphenyl congeners in sediment microcosms by two different Chloroflexi phylotypes. Appl Environ Microbiol 71:8085-8090 (Pubitemid 41803931)
20. Fagervold SK, May HD, Sowers KR (2007) Microbial reductive dechlorination of Aroclor 1260 in Baltimore harbor sediment microcosms is catalyzed by three phylotypes within the phylum Chloroflexi. Appl Environ Microbiol 73:3009-3018 (Pubitemid 46718585)
21. Fennell DE, Gossett JM, Zinder SH (1997) Comparison of butyric acid, ethanol, lactic acid, and propionic acid as hydrogen donors for the reductive dechlorination of tetrachloroethene. Environ Sci Technol 31:918-926 (Pubitemid 27106003)
22. Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Häggblom MM (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075-2081 (Pubitemid 38468808)
23. Field JA, Sierra-Alvarez R (2008) Microbial transformation and degradation of polychlorinated biphenyls. Environ Pollut 155:1-12 (Pubitemid 351899238)
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 (Pubitemid 47122586)
25. Futamata H, Yoshida N, Kurogi T, Kaiya S, Hiraishi A (2007) Reductive dechlorination of chloroethenes by Dehalococcoides-containing cultures enriched from a polychlorinated-dioxincontaminated microcosm. ISME J 1:471-479 (Pubitemid 47530653)
26. Häggblom MM (1992) Microbial breakdown of halogenated aromatic pesticides and related compounds. FEMS Microbiol Rev 9:29-71
27. He J, Sung Y, Krajmalnik-Brown R, Ritalahti KM, Löffler FE (2005) Isolation and characterization of Dehalococcoides sp. strain FL2, a trichloroethene (TCE)- and 1,2-dichloroethene-respiring anaerobe. Environ Microbiol 7:1442-1450 (Pubitemid 41204937)
28. Hendrickson ER, Payne JA, Young RM, Starr MG, Perry MP, Fahnestock S, Ellis DE, Ebersole RC (2002) Molecular analysis of Dehalococcoides 16S ribosomal DNA from chloroethene-contaminated sites throughout North America and Europe. Appl Environ Microbiol 68:485-495 (Pubitemid 34113032)
29. Himmelheber DW, Pennell KD, Hughes JB (2007) Natural attenuation processes during in situ capping. Environ Sci Technol 41:5306-5313 (Pubitemid 47221748)
30. Hiraishi A (2008) Biodiversity of dehalorespiring bacteria with special emphasis on polychlorinated biphenyl/dioxin dechlorinators. Microbes Environ 23:1-12
31. Hölscher T, Krajmalnik-Brown R, Ritalahti KM, Von Wintzingerode F, Görisch H, Löffler FE, Adrian L (2004) Multiple nonidentical reductive-dehalogenase-homologous genes are common in Dehalococcoides. Appl Environ Microbiol 70:5290-5297 (Pubitemid 39279602)
32. Kjellerup BV, Sun X, Ghosh U, May HD, Sowers KR (2008) Site-specific microbial communities in three PCB-impacted sediments are associated with different in situ dechlorinating activities. Environ Microbiol 10:1296-1309 (Pubitemid 351506332)
33. Krumins V, Park J-W, Son E, Rodenburg LA, Kerkhof LJ, Häggblom MM, Fennell DE (2009) Sustained PCB dechlorination enhancement in Anacostia river sediment. Water Res 43:4549-4558
34. Kube M, Beck A, Zinder SH, Kuhl H, Reinhardt R, Adrian L (2005) Genome sequence of the chlorinated compound-respiring bacterium Dehalococcoides species strain CBDB1. Nat Biotechnol 23:1269-1273
35. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons, New York, pp 115-175
36. Lendvay JM, Löffler FE, Dollhopf M, Aiello MR, Daniels G, Fathepure BG, Gebhard M, Heine R, Helton R, Shi J, Krajmalnik-Brown R, Major CL, Barcelona MJ, Petrovskis E, Hickey R, Tiedje JM, Adriaens P (2003) Bioreactive barriers: a comparison of bioaugmentation and biostimulation for chlorinated solvent remediation. Environ Sci Technol 37:1422-1431 (Pubitemid 36504962)
37. Liu F, Fennell DE (2008) Dechlorination and detoxification of 1,2,3,4,7,8-hexachlorodibenzofuran by a mixed culture containing Dehalococcoides ethenogenes strain 195. Environ Sci Technol 42:602-607
38. Löffler F, Cole JR, Ritalahti KM, Tiedje JM (2003) Diversity of dechlorinating bacteria. In: Häggblom MM, Bossert ID (eds) Dehalogenation: microbial processes and environmental applications. Kluwer Academic, Boston, pp 53-87
39. Major DW, McMaster ML, Cox EE, Edwards EA, Dworatzek SM, Hendrickson ER, Starr MG, Payne JA, Buonamici LW (2002) Field demonstration of successful bioaugmentation to achieve dechlorination of tetrachloroethene to ethene. Environ Sci Technol 36:5106-5116 (Pubitemid 35424849)
40. May HD, Miller GS, Kjellerup BV, Sowers KR (2008) Dehalorespiration with polychlorinated biphenyls by an anaerobic ultramicrobacterium. Appl Environ Microbiol 74:2089-2094 (Pubitemid 351522062)
41. McMurdie PJ, Behrens SF, Müller JA, Göke J, Ritalahti KM, Wagner R, Goltsman E, Lapidus A, Holmes S, Löffler FE, Spormann AM (2009) Localized plasticity in the streamlined genomes of vinyl chloride respiring Dehalococcoides. PLoS Genet 5:e1000714
42. 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 (Pubitemid 46079965)
43. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695-700 (Pubitemid 23072343)
44. Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW News 4:14
45. Nikolausz M, Chatzinotas A, Palatinszky M, Imfeld G, Martinez P, Kastner M (2008) Single-nucleotide primer extension assay for detection and sequence typing of "Dehalococcoides" spp. Appl Environ Microbiol 74:300-304
46. Park J-W, Crowley DE (2006) Dynamic changes in nahAc gene copy numbers during degradation of naphthalene in PAH-contaminated soils. Appl Microbiol Biotechnol 72:1322-1329 (Pubitemid 44564469)
47. Rahm BG, Richardson RE (2008) Dehalococcoides' gene transcripts as quantitative bioindicators of tetrachloroethene, trichloroethene, and cis-1,2-dichloroethene dehalorespiration rates. Environ Sci Technol 42:5099-5105
48. Rhee S-K, Fennell DE, Häggblom MM, Kerkhof LJ (2003) Detection of reductive dehalogenase motifs in PCR fragments from a sulfidogenic 2-bromophenol-degrading consortium enriched from estuarine sediment. FEMS Microbiol Ecol 43:317-324 (Pubitemid 36297066)
49. Seshadri R, Adrian L, Fouts DE, Eisen JA, Phillippy AM, Methe BA, Ward NL, Nelson WC, Deboy T, 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 PCE-dechlorinating bacterium Dehalococcoides ethenogenes. Science 307:105-108 (Pubitemid 40093488)
50. Shiang Fu Q, Barkovskii AL, Adriaens P (2005) Microbial dechlorination of dioxins in estuarine enrichment cultures: effects of respiratory conditions and priming compound on community structure and dechlorination patterns. Mar Environ Res 59:177-195 (Pubitemid 39310509)
51. Sung Y, Ritalahti KM, Apkarian RP, Löffler FE (2006) Quantitative PCR confirms purity of strain GT, a novel trichloroethene-toethene- respiring Dehalococcoides isolate. Appl Environ Microbiol 72:1980-1987
52. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599 (Pubitemid 47236692)
53. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882 (Pubitemid 28022245)
54. Vargas C, Fennell DE, Häggblom MM (2001) Anaerobic reductive dechlorination of chlorinated dioxins in estuarine sediments. Appl Microbiol Biotechnol 57:786-790 (Pubitemid 34028279)
55. Wagner A, Adrian L, Kleinsteuber S, Andreesen JR, Lechner U (2009) Transcription analysis of genes encoding homologues of reductive dehalogenases in "Dehalococcoides" sp. Strain CBDB1 by using terminal restriction fragment length polymorphism and quantitative PCR. Appl Environ Microbiol 75:1876-1884
56. 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 (Pubitemid 41803952)
57. Watts JE, Fagervold SK, May HD, Sowers KR (2005) A PCR-based specific assay reveals a population of bacteria within the Chloroflexi associated with the reductive dehalogenation of polychlorinated biphenyls. Microbiology 151:2039-2046 (Pubitemid 40909045)
58. Winchell LJ, Novak PJ (2008) Enhancing polychlorinated biphenyl dechlorination in fresh water sediment with biostimulation and bioaugmentation. Chemosphere 71:176-182 (Pubitemid 351231993)
59. Wittich RM (1998) Degradation of dioxin-like compounds by microorganisms. Appl Microbiol Biotechnol 49:489-499
60. Wu Q, Bedard DL, Wiegel J (1997) Temperature determines the pattern of anaerobic microbial dechlorination of Aroclor 1260 primed by 2,3,4,6-tetrachlorobiphenyl in Woods Pond sediment. Appl Environ Microbiol 63:4818-4825
61. Yan T, LaPara TM, Novak PJ (2006a) The reductive dechlorination of 2,3,4,5-tetrachlorobiphenyl in three different sediment cultures: evidence for the involvement of phylogenetically similar Dehalococcoides-like bacterial populations. FEMS Microbiol Ecol 55:248-261
62. Yan T, LaPara TM, Novak PJ (2006b) The effect of varying levels of sodium bicarbonate on polychlorinated biphenyl dechlorination in Hudson River sediment cultures. Environ Microbiol 8:1288-1298 (Pubitemid 43901759)
63. Yohda M, Kobayashi A, Ohishi S, Ebisawa M, Sakihara S, Kakihara F, Tojo Y, Tajima H, Nishimura M (2008) Quantitative discrimination of 16S rRNA genes of Dehalococcoides species by MagSNiPer, a quantitative single-nucleotide- polymorphism genotyping method. Biotechnol Appl Biochem 51:111-117
64. Yoshida N, Takahashi N, Hiraishi A (2005) Phylogenetic characterization of a polychlorinated-dioxin-dechlorinating microbial community by use of microcosm studies. Appl Environ Microbiol 71:4325-4334 (Pubitemid 41129483)