Advertisement

Diversity, Evolution, and Environmental Distribution of Reductive Dehalogenase Genes

  • Laura A. HugEmail author
Chapter

Abstract

Reductive dehalogenases, the active enzymes in organohalide respiration, are a diverse protein family with low sequence similarity and a punctuated distribution across the tree of life. The diversity, environmental distribution, and evolution of the reductive dehalogenases remain open questions. This chapter describes reductive dehalogenase sequence similarity and domain architecture, highlighting why predicting substrate specificity from sequence similarity is unreliable for these enzymes. Common in contaminated environments, but also identified in soda lakes, ocean sediment, and even as part of the human microbiome, the global distribution of reductive dehalogenases is broad and continually expanding. A map view of current locations where reductive dehalogenases have been detected provides compelling evidence for the ubiquity of these proteins in the environment, in keeping with predictions of an ancient origin for the group. The evolutionary history of the reductive dehalogenases includes vertical inheritance alongside a myriad of mechanisms for lateral transfer, including integrases, circularizing transposable elements, and, possibly, phage-mediated transfer. The reductive dehalogenases remain incompletely characterized from the perspectives of sequence diversity, substrate specificities, global distribution, and modes of inheritance.

Keywords

Reductive dehalogenase Evolution Substrate specificity Organohalide respiration Environmental distribution 

References

  1. Bondarev V, Richter M, Romano S et al (2013) The genus Pseudovibrio contains metabolically versatile bacteria adapted for symbiosis. Environ Microbiol 15:2095–2113. doi: 10.1111/1462-2920.12123 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Brouwer MSM, Warburton PJ, Roberts AP et al (2011) Genetic organisation, mobility and predicted functions of genes on integrated, mobile genetic elements in sequenced strains of Clostridium difficile. PLoS ONE 6:e23014. doi: 10.1371/journal.pone.0023014 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chen K, Huang L, Xu C et al (2013) Molecular characterization of the enzymes involved in the degradation of a brominated aromatic herbicide. Mol Microbiol 89:1121–1139. doi: 10.1111/mmi.12332 CrossRefPubMedGoogle Scholar
  4. DiDonato RJ, Young ND, Butler JE et al (2010) Genome sequence of the deltaproteobacterial strain NaphS2 and analysis of differential gene expression during anaerobic growth on naphthalene. PLoS ONE 5:e14072. doi: 10.1371/journal.pone.0014072 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Duhamel M, Edwards EA (2006) Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides. FEMS Microbiol Ecol 58:538–549. doi: 10.1111/j.1574-6941.2006.00191.x CrossRefPubMedGoogle Scholar
  6. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi: 10.1093/nar/gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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. doi: 10.1021/es960756r CrossRefGoogle Scholar
  8. Futagami T, Morono Y, Terada T et al (2009) Dehalogenation activities and distribution of reductive dehalogenase homologous genes in marine subsurface sediments. Appl Environ Microbiol 75:6905–6909. doi: 10.1128/AEM.01124-09 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Grostern A, Edwards EA (2006) Growth of Dehalobacter and Dehalococcoides spp. during degradation of chlorinated ethanes. Appl Environ Microbiol 72:428–436. doi: 10.1128/AEM.72.1.428-436.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  11. Hafenbradl D, Keller M, Dirmeier R et al (1996) Ferroglobus placidus gen. nov., sp. nov., A novel hyperthermophilic archaeum that oxidizes Fe2+ at neutral pH under anoxic conditions. Arch Microbiol 166:308–314CrossRefPubMedGoogle Scholar
  12. Hölscher T, Krajmalnik-Brown R, Ritalahti KM et al (2004) Multiple nonidentical reductive-dehalogenase-homologous genes are common in Dehalococcoides. Appl Environ Microbiol 70:5290–5297. doi: 10.1128/AEM.70.9.5290-5297.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hug LA, Edwards EA (2013) Diversity of reductive dehalogenase genes from environmental samples and enrichment cultures identified with degenerate primer PCR screens. Front Microbiol 4:341. doi: 10.3389/fmicb.2013.00341 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hug LA, Castelle CJ, Wrighton KC et al (2013a) Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1:22. doi: 10.1186/2049-2618-1-22 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hug LA, Maphosa F, Leys D et al (2013b) 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. doi: 10.1098/rstb.2012.0322 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Justicia-Leon SD, Ritalahti KM, Mack EE, Löffler FE (2012) Dichloromethane fermentation by a Dehalobacter sp. in an enrichment culture derived from pristine river sediment. Appl Environ Microbiol 78:1288–1291CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kaster A-K, Mayer-Blackwell K, Pasarelli B, Spormann AM (2014) Single cell genomic study of Dehalococcoidetes species from deep-sea sediments of the Peruvian Margin. ISME J 8:1831–1842. doi: 10.1038/ismej.2014.24 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kawai M, Futagami T, Toyoda A et al (2014) High frequency of phylogenetically diverse reductive dehalogenase-homologous genes in deep subseafloor sedimentary metagenomes. Front Microbiol 5:80. doi: 10.3389/fmicb.2014.00080 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kim S-H, Harzman C, Davis JK et al (2012) Genome sequence of Desulfitobacterium hafniense DCB-2, a Gram-positive anaerobe capable of dehalogenation and metal reduction. BMC Microbiol 12:21CrossRefPubMedPubMedCentralGoogle Scholar
  20. Krajmalnik-Brown R, Hölscher T, Thomson IN et al (2004) Genetic identification of a putative vinyl chloride reductase in Dehalococcoides sp. strain BAV1. Appl Environ Microbiol 70:6347–6351. doi: 10.1128/AEM.70.10.6347-6351.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Krajmalnik-Brown R, Sung Y, Ritalahti KM et al (2007) Environmental distribution of the trichloroethene reductive dehalogenase gene (tceA) suggests lateral gene transfer among Dehalococcoides. FEMS Microbiol Ecol 59:206–214. doi: 10.1111/j.1574-6941.2006.00243.x CrossRefPubMedGoogle Scholar
  22. Krzmarzick MJ, Crary BB, Harding JJ et al (2012) Natural niche for organohalide-respiring Chloroflexi. Appl Environ Microbiol 78:393–401. doi: 10.1128/AEM.06510-11 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Krzmarzick MJ, Miller HR, Yan T, Novak PJ (2014) Novel Firmicutes group implicated in the dechlorination of two chlorinated xanthones, analogues of natural organochlorines. Appl Environ Microbiol 80:1210–1218. doi: 10.1128/AEM.03472-13 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kube M, Beck A, Zinder SH et al (2005) Genome sequence of the chlorinated compound-respiring bacterium Dehalococcoides species strain CBDB1. Nat Biotechnol 23:1269–1273. doi: 10.1038/nbt1131 CrossRefPubMedGoogle Scholar
  25. Löffler FE, Sanford RA, Tiedje JM (1996) Initial characterization of a reductive dehalogenase from Desulfitobacterium chlororespirans Co23. Appl Environ Microbiol 62:3809–3813PubMedPubMedCentralGoogle Scholar
  26. Löffler FE, Yan J, Ritalahti KM et al (2012) Dehalococcoides mccartyi gen. nov., sp. nov., obligate organohalide-respiring anaerobic bacteria, relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidetes classis nov., within the phylum Chloroflexi. Int J Syst Evol Microbiol 63:625–635. doi: 10.1099/ijs.0.034926-0 CrossRefPubMedGoogle Scholar
  27. Lohner ST, Spormann AM (2013) Identification of a reductive tetrachloroethene dehalogenase in Shewanella sediminis. Philos Trans R Soc Lond B Biol Sci 368:20120326. doi: 10.1098/rstb.2012.0326 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mac Nelly A, Kai M, Svatoš A et al (2014) Functional heterologous production of reductive dehalogenases from Desulfitobacterium hafniense strains. Appl Environ Microbiol 80:4313–4322. doi: 10.1128/AEM.00881-14 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Magnuson JK, Stern RV, Gossett JM et al (1998) Reductive dechlorination of tetrachloroethene to ethene by a two-component enzyme pathway. Appl Environ Microbiol 64:1270–1275PubMedPubMedCentralGoogle Scholar
  30. Magnuson JK, Romine MF, Burris DR, Kingsley MT (2000) Trichloroethene reductive dehalogenase from Dehalococcoides ethenogenes: sequence of tceA and substrate range characterization. Appl Environ Microbiol 66:5141–5147CrossRefPubMedPubMedCentralGoogle Scholar
  31. Maillard J, Schumacher W, Vazquez F et al (2003) Characterization of the corrinoid iron-sulfur protein tetrachloroethene reductive dehalogenase of Dehalobacter restrictus. Appl Environ Microbiol 69:4628–4638CrossRefPubMedPubMedCentralGoogle Scholar
  32. Maillard J, Regeard C, Holliger C (2005) Isolation and characterization of Tn-Dha1, a transposon containing the tetrachloroethene reductive dehalogenase of Desulfitobacterium hafniense strain TCE1. Environ Microbiol 7:107–117. doi: 10.1111/j.1462-2920.2004.00671.x CrossRefPubMedGoogle Scholar
  33. Maphosa F, de Vos WM, Smidt H (2010) Exploiting the ecogenomics toolbox for environmental diagnostics of organohalide-respiring bacteria. Trends Biotechnol 28:308–316. doi: 10.1016/j.tibtech.2010.03.005 CrossRefPubMedGoogle Scholar
  34. Maphosa F, Lieten SH, Dinkla I et al (2012) Ecogenomics of microbial communities in bioremediation of chlorinated contaminated sites. Front Microbiol 3:351. doi: 10.3389/fmicb.2012.00351 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Marzorati M, de Ferra F, Van Raemdonck H et al (2007) A novel reductive dehalogenase, identified in a contaminated groundwater enrichment culture and in Desulfitobacterium dichloroeliminans strain DCA1, is linked to dehalogenation of 1,2-dichloroethane. Appl Environ Microbiol 73:2990–2999. doi: 10.1128/AEM.02748-06 CrossRefPubMedPubMedCentralGoogle Scholar
  36. McMurdie PJ, Behrens SF, Holmes S, Spormann AM (2007) Unusual codon bias in vinyl chloride reductase genes of Dehalococcoides species. Appl Environ Microbiol 73:2744–2747. doi: 10.1128/AEM.02768-06 CrossRefPubMedPubMedCentralGoogle Scholar
  37. McMurdie PJ, Behrens SF, Müller JA et al (2009) Localized plasticity in the streamlined genomes of vinyl chloride respiring Dehalococcoides. PLoS Genet 5:e1000714. doi: 10.1371/journal.pgen.1000714 CrossRefPubMedPubMedCentralGoogle Scholar
  38. McMurdie PJ, Hug LA, Edwards EA et al (2011) Site-specific mobilization of vinyl chloride respiration islands by a mechanism common in Dehalococcoides. BMC Genom 12:287. doi: 10.1186/1471-2164-12-287 CrossRefGoogle Scholar
  39. Müller JA, Rosner BM, Von Abendroth G et al (2004) Molecular identification of the catabolic vinyl chloride reductase from Dehalococcoides sp. strain VS and its environmental distribution. Appl Environ Microbiol 70:4880–4888. doi: 10.1128/AEM.70.8.4880-4888.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Neumann A, Scholz-Muramatsu H, Diekert G (1994) Tetrachloroethene metabolism of Dehalospirillum multivorans. Arch Microbiol 162:295–301CrossRefPubMedGoogle Scholar
  41. Neumann A, Wohlfarth G, Diekert G (1996) Purification and characterization of tetrachloroethene reductive dehalogenase from Dehalospirillum multivorans. J Biol Chem 271:16515–16519CrossRefPubMedGoogle Scholar
  42. Neumann A, Wohlfarth G, Diekert G (1998) Tetrachloroethene dehalogenase from Dehalospirillum multivorans: cloning, sequencing of the encoding genes, and expression of the pceA gene in Escherichia coli. J Bacteriol 180:4140–4145PubMedPubMedCentralGoogle Scholar
  43. Ni S, Fredrickson JK, Xun L (1995) Purification and characterization of a novel 3-chlorobenzoate-reductive dehalogenase from the cytoplasmic membrane of Desulfomonile tiedjei DCB-1. J Bacteriol 177:5135–5139PubMedPubMedCentralGoogle Scholar
  44. Nonaka H, Keresztes G, Shinoda Y et al (2006) Complete genome sequence of the dehalorespiring bacterium Desulfitobacterium hafniense Y51 and comparison with Dehalococcoides ethenogenes 195. J Bacteriol 188:2262–2274. doi: 10.1128/JB.188.6.2262-2274.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Padilla-Crespo E, Yan J, Swift C et al (2014) Identification and environmental distribution of dcpA, which encodes the reductive dehalogenase catalyzing the dichloroelimination of 1,2-dichloropropane to propene in organohalide-respiring Chloroflexi. Appl Environ Microbiol 80:808–818. doi: 10.1128/AEM.02927-13 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Peale JGD, Bakkom E, Lakhwala F et al (2008) TCE plume remediation via ISCR-enhanced bioremediation utilizing EHC® and KB-1®. Remediat J 18:19–31. doi: 10.1002/rem.20179 CrossRefGoogle Scholar
  47. Pöritz M, Goris T, Wubet T et al (2013) Genome sequences of two dehalogenation specialists—Dehalococcoides mccartyi strains BTF08 and DCMB5 enriched from the highly polluted Bitterfeld region. FEMS Microbiol Lett 343:101–104. doi: 10.1111/1574-6968.12160 CrossRefPubMedGoogle Scholar
  48. Regeard C, Maillard J, Holliger C (2004) Development of degenerate and specific PCR primers for the detection and isolation of known and putative chloroethene reductive dehalogenase genes. J Microbiol Methods 56:107–118CrossRefPubMedGoogle Scholar
  49. Rhee S-K, Fennell DE, Häggblom MM, Kerkhof LJ (2003) Detection by PCR of reductive dehalogenase motifs in a sulfidogenic 2-bromophenol-degrading consortium enriched from estuarine sediment. FEMS Microbiol Ecol 43:317–324. doi: 10.1111/j.1574-6941.2003.tb01072.x CrossRefPubMedGoogle Scholar
  50. Sattley WM, Blankenship RE (2010) Insights into heliobacterial photosynthesis and physiology from the genome of Heliobacterium modesticaldum. Photosynth Res 104:113–122. doi: 10.1007/s11120-010-9529-9 CrossRefPubMedGoogle Scholar
  51. Seshadri R, Adrian L, Fouts DE et al (2005) Genome sequence of the PCE-dechlorinating bacterium Dehalococcoides ethenogenes. Science 307:105–108. doi: 10.1126/science.1102226 CrossRefPubMedGoogle Scholar
  52. Sorokin DY, Tourova TP, Mussmann M, Muyzer G (2008) Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles 12:431–439. doi: 10.1007/s00792-008-0148-8 CrossRefPubMedGoogle Scholar
  53. Sung Y, Fletcher KE, Ritalahti KM et al (2006) Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl Environ Microbiol 72:2775–2782. doi: 10.1128/AEM.72.4.2775-2782.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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. doi: 10.1098/rstb.2012.0318 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Thole S, Kalhoefer D, Voget S et al (2012) Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life. ISME J 6:2229–2244. doi: 10.1038/ismej.2012.62 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Tsukagoshi N, Ezaki S, Uenaka T et al (2006) Isolation and transcriptional analysis of novel tetrachloroethene reductive dehalogenase gene from Desulfitobacterium sp. strain KBC1. Appl Microbiol Biotechnol 69:543–553. doi: 10.1007/s00253-005-0022-x CrossRefPubMedGoogle Scholar
  57. Von Wintzingerode F, Schlötelburg C, Hauck R et al (2001) Development of primers for amplifying genes encoding CprA- and PceA-like reductive dehalogenases in anaerobic microbial consortia, dechlorinating trichlorobenzene and 1,2-dichloropropane. FEMS Microbiol Ecol 35:189–196CrossRefGoogle Scholar
  58. Waller AS, Hug LA, Mo K et al (2012) Transcriptional analysis of a Dehalococcoides-containing microbial consortium reveals prophage activation. Appl Environ Microbiol 78:1178–1186. doi: 10.1128/AEM.06416-11 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wasmund K, Schreiber L, Lloyd KG et al (2014) Genome sequencing of a single cell of the widely distributed marine subsurface Dehalococcoidia, phylum Chloroflexi. ISME J 8:383–397. doi: 10.1038/ismej.2013.143 CrossRefPubMedGoogle Scholar
  60. West KA, Johnson DR, Hu P et al (2008) Comparative genomics of “Dehalococcoides ethenogenes” 195 and an enrichment culture containing unsequenced “Dehalococcoides” strains. Appl Environ Microbiol 74:3533–3540. doi: 10.1128/AEM.01835-07 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of WaterlooWaterlooCanada

Personalised recommendations