Organohalide-Respiring Deltaproteobacteria

  • Robert A. Sanford
  • Janamejaya Chowdhary
  • Frank E. LöfflerEmail author


Organohalide respiration was first discovered in the deltaproteobacterium Desulfomonile tiedjei, which used 3-chlorobenzoate as the respiratory electron acceptor. Since this breakthrough discovery, the organohalide-respiring phenotype was demonstrated in 6 out of the 21 currently published families of the class Deltaproteobacteria. A survey of 208 available deltaproteobacterial genome sequences identified putative reductive dehalogenase genes in about 10 % of the genomes, suggesting that the ability to perform reductive dechlorination is not rare among the Deltaproteobacteria. For example, free-living Geobacter lovleyi strains dechlorinate the priority pollutants tetrachloroethene and trichloroethene in freshwater aquifers whereas the sponge-associated species Desulfoluna spongiiphila uses bromo- and iodophenols as electron acceptors in marine environments. Organohalide-respiring Deltaproteobacteria inhabit diverse habitats where they fulfill key functions in the global cycling of halogens, and have relevant roles in bioremediation applications.


Electron Acceptor Reductive Dechlorination Reductive Dehalogenation Geobacter Sulfurreducens Reductive Dehalogenase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Ahn Y-B, Kerkhof LJ, Häggblom MM (2009) Desulfoluna spongiiphila sp. nov., a dehalogenating bacterium in the Desulfobacteraceae from the marine sponge Aplysina aerophoba. Int J Syst Evol Microbiol 59:2133–2139CrossRefPubMedGoogle Scholar
  2. Ahn YB, Rhee SK, Fennell DE, Kerkhof LJ, Hentschel U, Häggblom MM (2003) Reductive dehalogenation of brominated phenolic compounds by microorganisms associated with the marine sponge Aplysina aerophoba. Appl Environ Microbiol 69:4159–4166CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amos BK, Christ JA, Abriola LM, Pennell KD, Löffler F (2007a) Experimental evaluation and mathematical modeling of microbially enhanced tetrachloroethene (PCE) dissolution. Environ Sci Technol 41:963–970CrossRefPubMedGoogle Scholar
  4. Amos BK, Sung Y, Fletcher KE, Gentry TJ, Wu W-M, Criddle CS et al (2007b) Detection and quantification of Geobacter lovleyi strain SZ: implications for bioremediation at tetrachloroethene- and uranium-impacted sites. Appl Environ Microbiol 73:6898–6904CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bethke CM, Sanford RA, Kirk MF, Jin Q, Flynn TM (2011) The thermodynamic ladder in geomicrobiology. Am J Sci 311:183–210CrossRefGoogle Scholar
  6. Bommer M, Kunze C, Fesseler J, Schubert T, Diekert G, Dobbek H (2014) Structural basis for organohalide respiration. Science 346:455–458CrossRefPubMedGoogle Scholar
  7. Boyle AW, Phelps CD, Young LY (1999) Isolation from estuarine sediments of a Desulfovibrio strain which can grow on lactate coupled to the reductive dehalogenation of 2,4,6-tribromophenol. Appl Environ Microbiol 65:1133–1140PubMedPubMedCentralGoogle Scholar
  8. Buckel W, Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation. Biochim Biophys Acta 1827:94–113CrossRefPubMedGoogle Scholar
  9. Chen K, Huang L, Xu C, Liu X, He J, Zinder SH et al (2013) Molecular characterization of the enzymes involved in the degradation of a brominated aromatic herbicide. Mol Microbiol 89:1121–1139CrossRefPubMedGoogle Scholar
  10. Cole JR, Cascarelli AL, Mohn W, Tiedje J (1994) Isolation and characterization of a novel bacterium growing via reductive dehalogenation of 2-chlorophenol. Appl Environ Microbiol 60:3536–3542PubMedPubMedCentralGoogle Scholar
  11. Cole JR, Fathepure BZ, Tiedje J (1995) Tetrachloroethene and 3-chlorobenzoate dechlorination activities are co-induced in Desulfomonile tiedjei DCB-1. Biodegradation 6:167–172CrossRefPubMedGoogle Scholar
  12. de Jong E, Field JA, Spinnler H-E, Wijnberg JBPA, de Bont JAM (1994) Significant biogenesis of chlorinated aromatics by fungi in natural environments. Appl Environ Microbiol 60:264–270PubMedPubMedCentralGoogle Scholar
  13. De Wever H, Cole JR, Fettig MR, Hogan DA, Tiedje J (2000) Reductive dehalogenation of trichloroacetic acid by Trichlorobacter thiogenes gen. nov., sp. nov. Appl Environ Microbiol 66:2297–2301CrossRefPubMedPubMedCentralGoogle Scholar
  14. DeWeerd KA, Mandelco L, Tanner RS, Woese CR, Suflita J (1990) Desulfomonile tiedjei gen. nov. and sp. nov., a novel anaerobic, dehalogenating, sulfate-reducing bacterium. Arch Microbiol 154:23–30CrossRefGoogle Scholar
  15. DiDonato RJ, Young ND, Butler JE, Chin K-J, Hixson KK, Mouser P et al (2010) Genome sequence of the deltaproteobacterial strain NaphS2 and analysis of differential gene expression during anaerobic growth on naphthalene. PLoS ONE 5:e14072CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dolfing J, Novak I (2015) The Gibbs free energy of formation of halogenated benzenes, benzoates and phenols and their potential role as electron acceptors in anaerobic environments. Biodegradation 26:15–27CrossRefPubMedGoogle Scholar
  17. Dolfing J, Tiedje J (1987) Growth yield increase linked to reductive dechlorination in a defined 3-chlorobenzoate degrading methanogenic coculture. Arch Microbiol 149:102–105CrossRefPubMedGoogle Scholar
  18. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  19. Escalante-Semerena JC (2007) Conversion of cobinamide into adenosylcobamide in bacteria and archaea. J Bacteriol 189:4555–4560CrossRefPubMedPubMedCentralGoogle Scholar
  20. Fletcher KE, Costanza J, Pennell KD, Löffler FE (2011) Electron donor availability for microbial reductive processes following thermal treatment. Water Res 45:6625–6636CrossRefPubMedGoogle Scholar
  21. Flynn TM, O’Loughlin EJ, Mishra B, DiChristina TJ, Kemner KM (2014) Sulfur-mediated electron shuttling during bacterial iron reduction. Science 344:1039–1042CrossRefPubMedGoogle Scholar
  22. Garvie LAJ, Wilkens B, Groy TL, Glaeser JA (2015) Substantial production of drosophilin A methyl ether (tetrachloro-1,4-dimethoxybenzene) by the lignicolous basidiomycete Phellinus badius in the heartwood of mesquite (Prosopis juliflora) trees. Sci Nat 102:18CrossRefGoogle Scholar
  23. Gordon WG (2004) Amazing organohalogens: although best known as synthetic toxicants, thousands of halogen compounds are, in fact, part of our natural enviornment. Am Sci 92:342–349CrossRefGoogle Scholar
  24. Gribble GW (1994) The natural production of chlorinated compounds. Environ Sci Technol 28:310A–319ACrossRefPubMedGoogle Scholar
  25. Gribble GW (2000) The natural production of organobromine compounds. Environ Sci Pollut Res 7:37–47CrossRefGoogle Scholar
  26. Hatt JK, Ritalahti KM, Ogles DM, Lebrón CA, Löffler F (2013) Design and application of an internal amplification control to improve Dehalococcoides mccartyi 16S rRNA gene enumeration by qPCR. Environ Sci Technol 47:11131–11138CrossRefPubMedGoogle Scholar
  27. He JZ, Ritalahti KM, Yang KL, Koenigsberg SS, Löffler F (2003) Detoxification of vinyl chloride to ethene coupled to growth of an anaerobic bacterium. Nature 424:62–65CrossRefPubMedGoogle Scholar
  28. He Q, Sanford RA (2003) Characterization of Fe(III) reduction by chlororespiring Anaeromyxobacter dehalogenans. Appl Environ Microbiol 69:2712–2718CrossRefPubMedPubMedCentralGoogle Scholar
  29. He Q, Sanford RA (2004a) Acetate threshold concentrations suggest varying energy requirements during anaerobic respiration by Anaeromyxobacter dehalogenans. Appl Environ Microbiol 70:6940–6943CrossRefPubMedPubMedCentralGoogle Scholar
  30. He Q, Sanford RA (2004b) The generation of high biomass from chlororespiring bacteria using a continuous fed-batch bioreactor. Appl Microbiol Biotechnol 65:377–382CrossRefPubMedGoogle Scholar
  31. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28:1647–1649Google Scholar
  32. Keppler F, Borchers R, Pracht J, Rheinberger S, Schöler HF (2002) Natural formation of vinyl chloride in the terrestrial environment. Environ Sci Technol 36:2479–2483CrossRefPubMedGoogle Scholar
  33. Kim S-H, Harzman C, Davis J, Hutcheson R, Broderick J, Marsh T 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
  34. Krumholz L (1997) Desulfuromonas chloroethenica sp. nov. uses tetrachloroethylene and trichloroethylene as electron acceptors. Int J Syst Bacteriol 47:1262–1263CrossRefGoogle Scholar
  35. Krumholz L, Sharp R, Fishbain SS (1996) A freshwater anaerobe coupling acetate oxidation to tetrachloroethylene dehalogenation. Appl Environ Microbiol 62:4108–4113PubMedPubMedCentralGoogle Scholar
  36. Kudo K, Yamaguchi N, Makino T, Ohtsuka T, Kimura K, Dong DT et al (2013) Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1. Appl Environ Microbiol 79:4635–4642CrossRefPubMedPubMedCentralGoogle Scholar
  37. Löffler F, Ritalahti KM, Zinder SH (2013) Dehalococcoides and reductive dechlorination of chlorinated solvents. In: Stroo HF (ed) Bioaugmentation for groundwater remediation. Springer, New York, pp 39–88Google Scholar
  38. Löffler F, Tiedje J, Sanford RA (1999) Fraction of electrons consumed in electron acceptor reduction and hydrogen thresholds as indicators of halorespiratory physiology. Appl Environ Microbiol 65:4049–4056PubMedPubMedCentralGoogle Scholar
  39. Löffler FE, Sanford RA, Ritalahti KM (2005) Enrichment, cultivation, and detection of reductively dechlorinating bacteria. In: Jared RL (ed) Methods in Enzymology. Academic Press, New York, pp 77–111Google Scholar
  40. Lovley DR (1993) Dissimilatory metal reduction. Annu Rev Microbiol 47:263–290CrossRefPubMedGoogle Scholar
  41. Mahadevan R, Palsson BO, Lovley DR (2011) In situ to in silico and back: elucidating the physiology and ecology of Geobacter spp. using genome-scale modelling. Nat Rev Microbiol 9:39–50CrossRefPubMedGoogle Scholar
  42. Mohn W, Linkfield TG, Pankratz HS, Tiedje J (1990) Involvement of a collar structure in polar growth and cell division of strain DCB-1. Appl Environ Microbiol 56:1206–1211PubMedPubMedCentralGoogle Scholar
  43. Mohn W, Tiedje J (1991) Evidence for chemiosmotic coupling of reductive dechlorination and ATP synthesis in Desulfomonile tiedjei. Arch Microbiol 157:1–6CrossRefGoogle Scholar
  44. Neumann A, Wohlfarth G, Diekert G (1995) Properties of tetrachloroethene and trichloroethene dehalogenase of Dehalospirillum multivorans. Arch Microbiol 163:276–281CrossRefGoogle Scholar
  45. 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
  46. Nobu MK, Narihiro T, Hideyuki T, Qiu YL, Sekiguchi Y, Woyke T et al (2014) The genome of Syntrophorhabdus aromaticivorans strain UI provides new insights for syntrophic aromatic compound metabolism and electron flow. Environ Microbiol 17(12):4861–4872Google Scholar
  47. Odum JM, Singleton RJE (1993) The sulphate-reducing bacteria: contemporary perspectives. Springer-Verlag, New York. ISBN 0-387-97865-97868Google Scholar
  48. Ortiz-Bermudez P, Hirth KC, Srebotnik E, Hammel KE (2007) Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production. Proc Natl Acad Sci 104:3895–3900CrossRefPubMedPubMedCentralGoogle Scholar
  49. Parsons JR, Saez M, Dolfing J, de Voogt P (2008) Biodegradation of perfluorinated compounds. Rev Environ Contam Toxicol 196:53–71PubMedGoogle Scholar
  50. Payne KAP, Quezada CP, Fisher K, Dunstan MS, Collins FA, Sjuts H et al (2015) Reductive dehalogenase structure suggests a mechanism for B12-dependent dehalogenation. Nature 517:513–516CrossRefPubMedGoogle Scholar
  51. Sanford RA, Cole JR, Tiedje J (2002) Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl Environ Microbiol 68:893–900CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C et al (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci 109:19709–19714CrossRefPubMedPubMedCentralGoogle Scholar
  53. Shelton DR, Tiedje J (1984) Isolation and partial characterization of bacteria in an anaerobic consortium that mineralizes 3-chlorobenzoic acid. Appl Environ Microbiol 48:840–848PubMedPubMedCentralGoogle Scholar
  54. Slobodkina GB, Reysenbach AL, Panteleeva AN, Kostrikina NA, Wagner ID, Bonch-Osmolovskaya EA et al (2012) Deferrisoma camini gen. nov., sp. nov., a moderately thermophilic, dissimilatory iron(III)-reducing bacterium from a deep-sea hydrothermal vent that forms a distinct phylogenetic branch in the Deltaproteobacteria. Int J Syst Evol Microbiol 62:2463–2468CrossRefPubMedGoogle Scholar
  55. Smidt H, de Vos WM (2004) Anaerobic microbial dehalogenation. Annu Rev Microbiol 58:43–73CrossRefPubMedGoogle Scholar
  56. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30:1312–1313Google Scholar
  57. Stevens TO, Linkfield TG, Tiedje J (1988) Physiological characterization of strain DCB-1, a unique dehalogenating sulfidogenic bacterium. Appl Environ Microbiol 54:2938–2943PubMedPubMedCentralGoogle Scholar
  58. Suflita J, Horowitz A, Shelton DR, Tiedje J (1982) Dehalogenation: a novel pathway for the anaerobic biodegradation of haloaromatic compounds. Science 218:1115–1117CrossRefPubMedGoogle Scholar
  59. Sun B, Cole JR, Sanford RA, Tiedje J (2000) Isolation and characterization of Desulfovibrio dechloracetivorans sp. nov., a marine dechlorinating bacterium growing by coupling the oxidation of acetate to the reductive dechlorination of 2-chlorophenol. Appl Environ Microbiol 66:2408–2413CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sun B, Cole JR, Tiedje J (2001) Desulfomonile limimaris sp. nov., an anaerobic dehalogenating bacterium from marine sediments. Int J Syst Evol Microbiol 51:365–371CrossRefPubMedGoogle Scholar
  61. Sung Y, Fletcher K, Ritalahti KM, Apkarian RP, Ramos-Hernández N, Sanford RA et al (2006) Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl Environ Microbiol 72:2775–2782CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sung Y, Ritalahti KM, Sanford RA, Urbance JW, Flynn SJ, Tiedje J et al (2003) Characterization of two tetrachloroethene-reducing, acetate-oxidizing anaerobic bacteria and their description as Desulfuromonas michiganensis sp. nov. Appl Environ Microbiol 69:2964–2974CrossRefPubMedPubMedCentralGoogle Scholar
  63. Swan BK, Martinez-Garcia M, Preston CM, Sczyrba A, Woyke T, Lamy D et al (2011) Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333:1296–1300CrossRefPubMedGoogle Scholar
  64. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  65. Thomas SH, Sanford RA, Amos BK, Leigh MB, Cardenas E, Löffler F (2010) Unique ecophysiology among U(VI)-reducing bacteria as revealed by evaluation of oxygen metabolism in Anaeromyxobacter dehalogenans strain 2CP-C. Appl Environ Microbiol 76:176–183CrossRefPubMedGoogle Scholar
  66. Thomas SH, Wagner RD, Arakaki AK, Skolnick J, Kirby JR, Shimkets LJ et al (2008) The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria. PLoS ONE 3:e2103CrossRefPubMedPubMedCentralGoogle Scholar
  67. Treude N, Rosencrantz D, Liesack W, Schnell S (2003) Strain FAc12, a dissimilatory iron-reducing member of the Anaeromyxobacter subgroup of Myxococcales. FEMS Microbiol Ecol 44:261–269CrossRefPubMedGoogle Scholar
  68. Voordouw G (1995) The genus Desulfovibrio—the centennial. Appl Environ Microbiol 61:2813–2819PubMedPubMedCentralGoogle Scholar
  69. Wagner DD, Hug LA, Hatt JK, Spitzmiller MR, Padilla-Crespo E, Ritalahti KM et al (2012) Genomic determinants of organohalide-respiration in Geobacter lovleyi, an unusual member of the Geobacteraceae. BMC Genom 13:200CrossRefGoogle Scholar
  70. Wilson MC, Mori T, Rückert C, Uria AR, Helf MJ, Takada K et al (2014) An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature 506:58–62CrossRefPubMedGoogle Scholar
  71. Wöhlbrand L, Jacob JH, Kube M, Mussmann M, Jarling R, Beck A et al (2013) Complete genome, catabolic sub-proteomes and key-metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium. Environ Microbiol 15:1334–1355CrossRefPubMedGoogle Scholar
  72. Yan J, Im J, Yang Y, Löffler F (2013) Guided cobalamin biosynthesis supports Dehalococcoides mccartyi reductive dechlorination activity. Philos Trans R Soc B Biol Sci 368:20120320CrossRefGoogle Scholar
  73. Yan J, Ritalahti KM, Wagner DD, Löffler F (2012) Unexpected specificity of interspecies cobamide transfer from Geobacter spp. to organohalide-respiring Dehalococcoides mccartyi strains. Appl Environ Microbiol 78:6630–6636CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Robert A. Sanford
    • 1
  • Janamejaya Chowdhary
    • 2
  • Frank E. Löffler
    • 2
    • 3
    • 4
    Email author
  1. 1.Department of GeologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Biosciences DivisionOak Ridge National LaboratoryOak RidgeUSA
  3. 3.Joint Institute for Biological Sciences (JIBS)University of Tennessee and Oak Ridge National Laboratory (UT-ORNL)Oak RidgeUSA
  4. 4.Center for Environmental Biotechnology, Department of Microbiology, Department of Civil and Environmental EngineeringUniversity of TennesseeKnoxvilleUSA

Personalised recommendations