Skip to main content
SpringerLink
Log in

Microbial consortia involved in the anaerobicdegradation of hydrocarbons

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

In this review, we examine the energetics of well-characterized biodegradation pathways and explore the possibilities for these to support growth of multiple organisms interacting in consortia. The relevant phenotypic and/or phylogenetic characteristics of isolates and consortia mediating hydrocarbon degradation coupled with different terminal electron-acceptingprocesses (TEAP) are also reviewed. While the information on metabolic pathways has been gained from the analysis of individual isolates, the energetic framework presented here demonstrates that microbial consortia could be readily postulated for hydrocarbon degradation coupled to any TEAP. Several specialized reactions occur within these pathways, and the organisms mediating these are likely to play a key role in defining the hydrocarbon degradation characteristics of the community under a given TEAP. Comparing these processes within and between TEAPs reveals biological unity in that divergent phylotypes display similar degradation mechanisms and biological diversity in that hydrocarbon-degraders closely related as phylotypes differ in the type and variety of hydrocarbon degradation pathways they possess. Analysis of microcosms and of field samples suggests that we have only begun to reveal the diversity of organisms mediating anaerobic hydrocarbon degradation. Advancements in the understanding of how hydrocarbon-degrading communities function will be significantly affected by the extent to which organisms mediating specialized reactions can be identified, and tools developed to allow their study in situ.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aeckersberg F, Bak F & Widdel F (1991) Anaerobic oxidation of saturated hydrocarbons to CO2 by a new type of sulfate-reducing bacterium. Arch. Microbiol. 156: 5–14

    Google Scholar 

  • Aeckersberg F, Rainey FA & Widdel F (1998) Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch. Microbiol. 170: 361–369

    Google Scholar 

  • Anderson RT & Lovley DR (1997). Ecology and biogeochemistry of in situ groundwater bioremediation. In: Jones JG (Ed) Advances in Microbial Ecology, Vol 15(pp 289–331). New York, Plenum Press

    Google Scholar 

  • Archer DB & Harris JE (1986). Methanogenic bacteria and methane production in various habitats. In: Burnes EM and Mead GC (Eds) Anaerobic bacteria in habitats other than man (pp 185–223). Boston, Blackwell Scientific

    Google Scholar 

  • Ball HA, Johnson HA, Reinhard M & Spormann AM (1996) Initial reactions in anaerobic ethylbenzene oxidation by a denitrifying bacterium, strain EB1. J. Bacteriol. 178: 5755–5761

    Google Scholar 

  • Ball HA & Reinhard M (1996) Monoaromatic hydrocarbon transformation under anaerobic conditions at Seal Beach, California: Laboratory studies. Environ. Sci. Technol. 15: 114–122

    Google Scholar 

  • Bekins BA, Godsy EM & Warren E (1999) Distribution of microbial physiologic types in an aquifer contaminated by crude oil. Microb. Ecol. 37: 263–273

    Google Scholar 

  • Beller HR& Spormann AM(1997a) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J. Bacteriol. 179: 670–676

    Google Scholar 

  • Beller HR& Spormann AM(1997b) Benzylsuccinate formation as a means of anaerobic toluene activation by sulfate-reducing strain PRTOL1. Appl Environ Microbiol 63: 3729–3731

    Google Scholar 

  • Boll M & Fuchs G (1998) Identification and characterization of the natural electron donor ferredoxin and of FAD as a possible prosthetic group of benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic metabolism. Eur. J. Biochem. 251: 946–954

    Google Scholar 

  • Borden RC, Hunt MJ, Shafer MB & Barlaz MA (1997) Anaerobic biodegradation of BTEX in aquifer material. United States Environmental Protection Agency, Ada, OK

    Google Scholar 

  • Caldwell DE, Wolfaardt GM, Korber DR & Lawrence JR (1997). Do bacterial communities transcend Darwinism? In: Jones JG (Ed) Advances in Microbial Ecology, Vol 15(pp 105–175). New York, Plenum Press

    Google Scholar 

  • Chapelle FH & Lovley DR (1992) Competitive exclusion of sulfate reduction by Fe(III)-reducing bacteria: a mechanism for producing discrete zones of high-iron ground water. Ground Water 30: 29–36

    Google Scholar 

  • Chapelle FH, McMahon PB, Dubrovsky NM, Fujii RF, Oaksford ET & Vroblesky DA (1995) Deducing the distribution of terminal electron-accepting processes in hydrologically diverse groundwater systems. Water Resources Research 31: 359–371

    Google Scholar 

  • Coates JD, Phillips EJP, Lonergan DJ, Jenter H & Lovley DR (1996) Isolation of Geobacter species from diverse sedimentary environments. Appl. Environ. Microbiol. 62: 1531–1536

    Google Scholar 

  • Dojka M, Hungenholtz P, Haack S & Pace N (1998) Microbial diversity in a hydrocarbon-and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64: 3869–3877

    Google Scholar 

  • Dolfing J, Zeyer J, Binder-Eicher P & Schwarzenbach RP (1990) Isolation and characterization of a bacterium that mineralizes toluene in the absence of molecular oxygen. Arch. Microbiol. 154: 336–341

    Google Scholar 

  • Edwards EA & Grbi´c-Gali´c D (1992) Complete mineralization of benzene by aquifer microorganisms under strictly anaerobic conditions. Appl. Environ. Microbiol. 58: 2663–2666

    Google Scholar 

  • Edwards EA & Grbi´c-Gali´c D (1994) Anaerobic degradation of toluene and o-xylene by a methanogenic consortium. Appl. Environ. Microbiol. 60: 313–322

    Google Scholar 

  • Edwards EA, Wills LE & Grbi´c-Gali´c D (1992) Anaerobic degradation of toluene and xylene by aquifer microorganisms under sulfate-reducing conditions. Appl. Environ. Microbiol. 58: 794–800

    Google Scholar 

  • Fernandez A, Huang SY, Seston S, Xing J, Hickey R, Criddle C & Tiedje J (1999) How stable is stable? Function versus community composition. Appl. Environ. Microbiol. 65: 3697–3704

    Google Scholar 

  • Ficker M, Krastel K, Orlicky S & Edwards E (1999) Molecular characterization of a toluene-degrading methanogneic consortium. Appl. Environ. Microbiol. 65: 5576–5585

    Google Scholar 

  • Fries MR, Zhou J, Chee-Sanford J & Tiedje JM (1994) Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitats. Appl. Environ. Microbiol. 60: 2802–2810

    Google Scholar 

  • Garcia JL (1990) Taxonomy and ecology of methanogens. Microbial Reviews 87: 297–308

    Google Scholar 

  • Harms G, Rabus R & Widdel F (1999a) Anaerobic oxidation of the aromatic plant hydrocarbon p-cymene by newly isolated denitrifying bacteria. Arch. Microbiol. 172: 303–312

    Google Scholar 

  • Harms G, Zengler K, Rabus R, Aeckersberg F, Minz D, Rosselló-Mora R & Friedrich W(1999b) Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria. Appl. Environ. Microbiol. 65: 999-1004

    Google Scholar 

  • Harris RF (1982). Energetics of nitrogen transformations. In: Stevenson FJ, Bremner JM, Hauck RD and Keeney DR (Eds) Nitrogen in Agricultural Soils. Agronomy Monograph, No. 22 (pp 833–890). Madison, WI, American Society of Agronomy

    Google Scholar 

  • Harris RF & Arnold SM (1995). Redox and energy aspects of soil bioremediation In: Bioremediation: Science and Applications (pp 55–85). Soil Science Society of America, Madison, WI

    Google Scholar 

  • Harwood CS, Burchhardt G, Herrmann H & Fuchs G (1999) Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol. Rev. 22: 439–458

    Google Scholar 

  • Heider J & Fuchs G (1997) Microbial anaerobic aromatic metabolism. Anaerobe 3: 1–22

    Google Scholar 

  • Heider J, Spormann AM, Beller HR & Widdel F (1999) Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol. Rev. 22: 459–473

    Google Scholar 

  • Hess A, Zarda B, Hahn D, Häner A, Stax D, Hähemer P & Zeyer J (1997) In situ analysis of denitrifying toluene-and m-xylene-degrading bacteria in a diesel fuel-contaminated laboratory aquifer column. Appl. Environ. Microbiol. 63: 2136–2141

    Google Scholar 

  • Holt JG, Krieg NR, Sneath PHA, Staley JT & Williams ST (Eds) (1994) Bergey's Manual of Determinative Bacteriology. Williams & Wilkins, Philadelphia

    Google Scholar 

  • Hutchins SR (1991) Optimizing BTEX biodegradation under denitrifying conditions. Environ. Toxicol. Chem. 10: 1437–1448

    Google Scholar 

  • Hutchins SR (1997) Effects of microcosm preparation on rates of toluene biodegradation under denitrifying conditions. J. Ind. Microbiol. Biotechnol. 18: 170–176

    Google Scholar 

  • Hutchins SR, Miller DE & Thomas A (1998) Combined laboratory/ field study on the use of nitrate for in situ bioremediation of a fuel-contaminated aquifer. Environ. Sci. Technol. 21: 1832–1840

    Google Scholar 

  • Kafkewitz D & Togna MT (1998). Microbes in the muck: a look into the anaerobic world. In: Lewandowski GA and DeFilippi LJ (Eds) Biological Treatment of Hazardous Wastes (pp 327–356). John Wiley & Sons, Inc, New York

    Google Scholar 

  • Kazumi J, Caldwell ME, Suflita JM, Lovley DR & Young LY (1997) Anaerobic degradation of benzene in diverse anoxic environments. Environ. Sci. Technol. 31: 813–818

    Google Scholar 

  • Krieger CJ, Beller HR, Reinhard M & Spormann AM (1999) Initial reactions in anaerobic oxidation of m-xylene by the denitrifying bacterium Azoarcus sp. strain T. J. Bacteriol. 181: 6403–6410

    Google Scholar 

  • Lonergan DJ, Jenter HL, Coates JD, Phillips EJP, Schmidt TM & Lovley DR (1996) Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J. Bacteriol. 178: 2402–2408

    Google Scholar 

  • Lovely DR, Fraga JL, Coates J, D. & Blunt-Harris EL (1999) Humics as an electron donor for anaerobic respiration. Environ. Microbiol. 1: 89–98

    Google Scholar 

  • Lovely DR & Phillips EJP (1988) Movel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54: 1472–1480

    Google Scholar 

  • Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbial. Rev. 55: 259–287

    Google Scholar 

  • Lovley DR (1997) Potential for anaerobic bioremediation of BTEX in petroleum-contaminated aquifers. J. Ind. Microbiol. Biotechnol. 18: 75–81

    Google Scholar 

  • Lovley DR (1998) Geomicrobiology: Interactions between microbes and minerals. Science 280: 54–55

    Google Scholar 

  • Lovley DR, Chapelle FH & Woodward JC (1994a) Use of dissolved H2 concentrations to determine distribution of microbially catalyzed redox reactions in anoxic groundwater. Environ. Sci. Technol. 28: 1205–1210

    Google Scholar 

  • Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EP, Gorby YA & Goodwin S (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 159: 336–344

    Google Scholar 

  • Lovley DR & Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl. Environ. Microbiol. 56: 1858–1864

    Google Scholar 

  • Lovley DR & Phillips EJP (1989) Requirement for a microbial consortium to completely oxidize glucose in Fe(III)-reducing sediments. Appl. Environ. Microbiol. 55: 3234–3236

    Google Scholar 

  • Lovley DR & Woodward JC (1996) Mechanisms for chelator stimulation of microbial Fe(III)-oxide reduction. Chem. Ecol. 132: 19–24

    Google Scholar 

  • Lovley DR, Woodward JC & Chapelle FH (1994b) Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe(III) ligands. Nature 370: 128–131

    Google Scholar 

  • Lovley DR, Woodward JC & Chapelle FH (1996) Rapid anaerobic benzene oxidation with a variety of chelated Fe(III) forms. Appl. Environ. Microbiol. 62: 288–291

    Google Scholar 

  • Ludvigsen L, Albrechtsen H-J, Ringelberg DB, Ekelund F & Christensen TH (1999) Distribution and composition of microbial populations in a landfill leachate contaminated aquifer (Grindsted, Denmark). Microb. Ecol. 37: 197–207

    Google Scholar 

  • Meckenstock RU (1999) Fermentative toluene degradation in anaerobic defined syntrophic cocultures. FEMS Microbiol. Lett. 177: 67–73

    Google Scholar 

  • Muyzer G, Hottenträger S, Teske A & Wawer C (1996). Denaturing gradient gel electrophoresis of PCR-amplified 16S rDNA – A new molecular approach to analyse the genetic diversity of mixed microbial communities. In: Akkermans ADL, van Elsas JD and FJ dB (Eds) Molecular Microbial Ecology Manual (3.4.4: pp 1–27). Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Muyzer G & Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73: 127–141

    Google Scholar 

  • Muyzer G, 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

    Google Scholar 

  • Nales M, Butler BJ & Edwards EA (1998) Anaerobic benzene biodegradation: a microcosm survey. Bioremediation J. 2: 125–144

    Google Scholar 

  • Oremland RS (1988). Biogeochemistry of methanogenic bacteria In: Zehnder AJB (Ed) Biology of Anaerobic Microorganisms (pp 641–706). New York, John Wiley & Sons

    Google Scholar 

  • Phelps CD, Kerkhof LJ & Young LY (1998) Molecular characterization of a sulfate-reducing consortium which mineralizes benzene. FEMS Microbiol. Ecol. 27: 269–279

    Google Scholar 

  • Phelps CD & Young LY (1999) Anaerobic biodegradation of BTEX and gasoline in various aquatic sediments. Biodegradation 10: 15–25

    Google Scholar 

  • Rabus R& Heider J (1998) Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulfate reducing bacteria. Arch. Microbiol. 170: 377–384

    Google Scholar 

  • Rabus R & Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch. Microbiol. 163: 96–103 158

    Google Scholar 

  • Reinhard M, Shang S, Kitanidis PK, Orwin E, Hopkins GD & Lebron CA (1997) In situ BETX biotransformation under enhanced nitrate-and sulfate-reducing conditions. Environ. Sci. Technol. 31: 28–36

    Google Scholar 

  • Richardson DJ (2000) Bacterial respiration: a flexible process for a changing environment. Microbiology 146: 551–571

    Google Scholar 

  • Rooney-Varga JN, Anderson RT, Fraga JL, Ringelberg D & Lovley DR (1999) Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 65: 3056–3063

    Google Scholar 

  • Rueter P, Rabus R, Wilkes H, Aeckersberg F, Rainey FA, Jannasch H & Widdel F (1994) Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 372: 455–458

    Google Scholar 

  • Salanitro JP, Wisniewski HL, Byers DL, Neaville CC & Schroder RA (1997) Use of aerobic and anaerobic microcosms to assess BTEX biodegradation in aquifers. Groundwater Monitoring and Remediation 17: 210–221

    Google Scholar 

  • Schocher RJ, Seyfried B, Vazquez F & Zeyer J (1991) Anaerobic degradation of toluene by pure cultures of denitrifying bacteria. Arch. Microbiol. 157: 7–12

    Google Scholar 

  • Shi Y, Zwolinski MD, Schreiber ME, Bahr JM, Sewell GW & Hickey WJ (1999) Molecular analysis of microbial community structure in pristine and contaminated aquifers: field and laboratory microcosm studies. Appl. Environ. Microbiol. 65: 2143–2150

    Google Scholar 

  • Shlomi ER, Lankhorst A & Prins RA (1978) Methanogenic fermentation of benzoate in an enrichment culture. Microb. Ecol. 4: 249–261

    Google Scholar 

  • So CM & Young LY (1999) Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl. Environ. Microbiol. 65: 2969–2976

    Google Scholar 

  • Song B, Häggblom MM, Zhou J, Tiedje JM & Palleroni NJ (1999) Taxonomic characterization of denitrifying bacteria that degrade aromatic compounds and description of Azoarcus toluvorans sp. nov. and Azoarcus toluclasticus sp. Nov. Int. J. Syst. Bacteriol. 49: 1129–1140

    Google Scholar 

  • Stouthamer AH (1988). Dissimilatory reduction of oxidized nitrogen compounds. In: Zehnder AJB (Ed) Biology of Anaerobic Microorganisms (pp 245–303). John Wiley & Sons, New York

    Google Scholar 

  • Thauer RK, Jungerman K & Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41: 100-180

    Google Scholar 

  • Thomas JM, Bruce CL, Gordy VR, Duston KL, Hutchins SR, Sinclair JL & Ward CH (1997) Assessment of the microbial potential for nitrate-enhanced bioremediation of a JP-4 fuelcontaminated aquifer. J. Ind. Microbiol. Biotechnol. 18: 213–221

    Google Scholar 

  • Tiedje JM (1988). Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (Ed) Biology of Anaerobic Microorganisms (pp 179–244). John Wiley & Sons, New York

    Google Scholar 

  • Vroblesky DA & Chapell FH (1994) Temporal and spatial changes of terminal electron-accepting processes in a petroleum hydrocarbon-contaminated aquifer and the significance for contaminant biodegradation. Water Res. Res. 30: 1561-157

    Google Scholar 

  • Weiner JM, Lauck TS & Lovley DR (1998) Enhanced anaerobic benzene degradation with the addition of sulfate. Bioremediation J. 2: 159–173

    Google Scholar 

  • Weiner JM& Lovley DR (1998a) Anaerobic benzene degradation in petroleum-contaminated aquifer sediments after inoculation with a benzene-oxidizing enrichment. Appl. Environ. Microbiol. 64: 775–778

    Google Scholar 

  • Weiner JM & Lovley DR (1998b) Rapid benzene degradation in methanogenic sediments from a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 64: 1937–1939

    Google Scholar 

  • Widdel F (1988) Microbiology and ecology of sulfate-and sulferreducing bacteria. In: Zehnder AJB (Ed) Biology of Anaerobic Microorganisms (pp 469–585). John Wiley and Sons, New York

    Google Scholar 

  • Zehnder AJB & Stumm W (1988). Geochemistry and biogeochemistry of anaerobic habitats. In: Zehnder AJB (Ed) Biology of Anaerobic Microorganisms (pp 1–38). John Wiley & Sons, New York

    Google Scholar 

  • Zengler K, Richnow HH, Rosselló-Mora R, Michaelis W & Widdel F (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401: 266–269

    Google Scholar 

  • Zhou J, Fries MR, Chee-Sanford JC & Tiedje JM (1995) Phylogenetic analysis of a new group of denitrifiers capable of anaerobic growth on toluene and description of Azoarcus tolulyticus sp. Nov. Int. J. Syst. Bacteriol. 45: 500–506

    Google Scholar 

  • Zumft WG (1992). The denitrifying prokaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer K-H (Eds) The Prokaryotes, Vol 1(pp 554–582). Springer-Verlag, New York

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Environmental Toxicology Center, University of Wisconsin-Madison, Madison, WI, 53706-1299, USA

    M.D. Zwolinski

  2. Environmental Toxicology Center and Department of Soil Science, University of Wisconsin-Madison, Madison, WI, 53706-1299, USA

    R.F. Harris

  3. Environmental Toxicology Center and Department of Soil Science, University of Wisconsin-Madison, Madison, WI, 53706-1299, USA.

    W.J. Hickey

Authors
  1. M.D. Zwolinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R.F. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W.J. Hickey
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zwolinski, M., Harris, R. & Hickey, W. Microbial consortia involved in the anaerobicdegradation of hydrocarbons. Biodegradation 11, 141–158 (2000). https://doi.org/10.1023/A:1011190316012

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011190316012

Search

Navigation