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Journal of Environmental Science and Health, Part A
Toxic/Hazardous Substances and Environmental Engineering
Volume 54, 2019 - Issue 5
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Articles

Aerobic and anaerobic enrichment cultures highlight the pivotal role of facultative anaerobes in soil hydrocarbon degradation

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Pages 408-415 | Received 03 Aug 2018, Accepted 01 Dec 2018, Published online: 24 Jan 2019

References

  • Atlas, R. M. Microbial Degradation of Petroleum Hydrocarbons: An Environmental Perspective. Microbiol. Rev. 1981, 45, 180–209.
  • Leahy, J. G.; Colwell, R. R. Microbial Degradation of Hydrocarbons in the Environment. Microbiol. Rev. 1990, 54, 305–315.
  • Smith, M. R. The Biodegradation of Aromatic Hydrocarbons by Bacteria. Biodegradation 1990, 1, 191–206.
  • Atlas, R. M.; Bartha, R. Hydrocarbon Biodegradation and Oil Spill Bioremediation. Adv. Microb. Ecol. 1992, 12, 287–338.
  • Cerniglia, C. E. Biodegradation of Polycyclic Aromatic Hydrocarbons. Biodegradation 1992, 3, 351–368. DOI: 10.1007/BF00129093.
  • Van Hamme, J. D.; Singh, A.; Ward, O. P. Recent Advances in Petroleum Microbiology. Microbiol. Mol. Biol. Rev. 2003, 67, 503–549. DOI: 10.1128/MMBR.67.4.503-549.2003.
  • Das, N.; Chandran, P. Microbial Degradation of Petroleum Hydrocarbon Contaminants: An Overview. Biotechnol. Res. Int. 2011, 2011, 1. ID. 941810. DOI: 10.4061/2011/941810.
  • Fritsche, W.; Hofrichter, M. Aerobic Degradation by Microorganisms. In Environmental Processes – Soil Decontamination; Klein, J., Ed.; Wiley-VCH Verlag GmbH: Weinheim, Germany, 2000; pp 146–155.
  • Meckenstock, R. U.; Mouttaki, H. Anaerobic Degradation of Non-substituted Aromatic Hydrocarbons. Curr. Opin. Biotechnol. 2011, 22, 406–414.
  • Canfield, D. E.; Kristensen, E.; Thamdrup, B. Aquatic Geomicrobiology. Adv. Mar. Biol. 2005, 48, 1–599.
  • Lovley, D. R.; Phillips, E. J. P. Novel Processes for Anaerobic Sulfate Production from Elemental Sulfur by Sulfate-Reducing Bacteria. Appl. Environ. Microbiol. 1994, 60, 2394–2399.
  • Austin, R. N.; Callaghan, A. V. Microbial Enzymes That Oxidize Hydrocarbons. Front. Microbiol. 2013, 4, 338.
  • Heider, J.; Schühle, K. Anaerobic Biodegradation of Hydrocarbons Including Methane. In The Prokaryotes: Prokaryotic Physiology and Biochemistry; Rosenberg, E.; DeLong, E. F.; Thompson, F.; Lory, S.; Stackebrandt, E., Eds.; Springer-Verlag: Berlin Heidelberg, 2013; pp. 605–634.
  • Rabus, R.; Boll, M.; Heider, J.; Meckenstock, R. U.; Buckel, W.; Einsle, O.; Ermler, U.; Golding, B. T.; Gunsalus, R. P.; Kroneck, P. M. H.; et al. Anaerobic Microbial Degradation of Hydrocarbons: From Enzymatic Reactions to the Environment. J. Mol. Microbiol. Biotechnol. 2016, 26, 5–28. DOI: 10.1159/000443997.
  • Fukui, M.; Harms, G.; Rabus, R.; Schramm, A.; Widdel, F.; Zengler, K.; Boreham, C.; Wilkes, H. Anaerobic Degradation of Oil Hydrocarbons by Sulfate-Reducing and Nitrate-Reducing Bacteria. In Microbial Ecology of Oil Fields; Proceedings of the 8th International Symposium on Microbial Ecology; Bell, C.R.; Brylinsky, M.; Johnson-Green, P., Eds.; Atlantic Canada Society for Microbial Ecology: Halifax, Canada, 1999; p. 199.
  • So, C. M.; Young, L. Y. Isolation and Characterization of a Sulfate-Reducing Bacterium That Anaerobically Degrades Alkanes. Appl. Environ. Microbiol. 1999, 65, 2969–2976.
  • Annweiler, E.; Materna, A.; Safinowski, M.; Kappler, A.; Richnow, H. H.; Michaelis, W.; Meckenstock, R. U. Anaerobic Degradation of 2-Methylnaphthalene by a Sulfate-Reducing Enrichment Culture. Environ. Microbiol. 2000, 66, 5329–5333. DOI: 10.1128/AEM.66.12.5329-5333.2000.
  • Coates, J. D.; Chakraborty, R.; Lack, J. G.; O’Connor, S. M.; Cole, K. A.; Bender, K. S.; Achenbach, L. A. Anaerobic Benzene Oxidation Coupled to Nitrate Reduction in Pure Culture by Two Strains of Dechloromonas. Nature 2001, 411, 1039–1044. DOI: 10.1038/35082545.
  • Chakraborty, R.; Coates, J. D. Hydroxylation and Carboxylation − Two Crucial Steps of Anaerobic Benzene Degradation by Dechloromonas Strain RCB. Appl. Environ. Microbiol. 2005, 71, 5427–5432. DOI: 10.1128/AEM.71.9.5427-5432.2005.
  • Callaghan, A. V.; Tierney, M.; Phelps, C. D.; Young, L. Y. Anaerobic Biodegradation of n-hexadecane by a Nitrate-reducing Consortium. Appl. Environ. Microbiol. 2009, 75, 1339–1344. DOI: 10.1128/AEM.02491-08.
  • Callaghan, A. V.; Morris, B. E. L.; Pereira, I. A. C.; McInerney, M. J.; Austin, R. N.; Groves, J. T.; Kukor, J. J.; Suflita, J. M.; Young, L. Y.; Zylstra, G. J.; Wawrik, B. The Genome Sequence of Desulfatibacillum alkenivorans AK-01: A Blueprint for Anaerobic Alkane Oxidation. Environ. Microbiol. 2012, 14, 101–113. DOI: 10.1111/j.1462-2920.2011.02516.x.
  • Bushnell, L. D.; Haas, H. F. The Utilization of Certain Hydrocarbons by Microorganisms. J. Bacteriol. 1941, 41, 653–673.
  • Eriksson, M.; Sodersten, E.; Yu, Z.; Dalhammar, G.; Mohn, W. W. Degradation of Polycyclic Aromatic Hydrocarbons at Low Temperature under Aerobic and Nitrate-reducing Conditions in Enrichment Cultures from Northern Soils. Appl. Environ. Microbiol. 2003, 69, 275–284. DOI: 10.1128/AEM.69.1.275-284.2003.
  • Taylor, C.; Chen, R. T. Thermophilic Biodegradation of BTEX by Two Consortia of Anaerobic Bacteria. Appl. Microbiol. Biotechnol. 1997, 48, 121–128. DOI: 10.1007/s002530051026.
  • Mittal, M.; Rockne, K. J. Indole Production by Pseudomonas stutzeri Strain NAP-3 during Anaerobic Naphthalene Biodegradation in the Presence of Dimethyl Formamide. J. Environ. Sci. Health. A Tox. Hazard. Subst. Environ. 2008, 43, 1027–1034. DOI: 10.1080/10934520802059896.
  • Edwards, E. A.; Grbić-Galić, D. Grbić-Galić, D. Anaerobic Degradation of Toluene and o-xylene by a Methanogenic Consortium. Appl. Environ. Microbiol. 1994, 60, 313–322.
  • Widdel, F.; Pfennig, N. Studies on Dissimilatory Sulfate-reducing Bacteria That Decompose Fatty Acids. Isolation of New Sulfate-reducing Bacteria Enriched with Acetate from Saline Environments. Arch. Microbiol. 1981, 129, 395–400. DOI: 10.1007/BF00406470.
  • Dou, J.; Liu, X.; Ding, A. Anaerobic Degradation of Naphthalene by the Mixed Bacteria Under Nitrate Reducing Conditions. J. Hazard. Mater. 2009, 165, 325–331. DOI: 10.1016/j.jhazmat.2008.10.002.
  • Palanisamy, N.; Ramya, J.; Kumar, S.; Vasanthi, N.; Chandran, P.; Khan, S. Diesel Biodegradation Capacities of Indigenous Bacterial Species Isolated from Diesel Contaminated Soil. J. Environ. Health. Sci. Eng. 2014, 12, 142.
  • Kolmert, Å.; Wikström, P.; Hallberg, K. B. A Fast and Simple Turbidimetric Method for the Determination of Sulfate in Sulfate-reducing Bacterial Cultures. J. Microbiol. Methods 2000, 41, 179–184. DOI: 10.1016/S0167-7012(00)00154-8.
  • Bartholomew, J. W.; Mittwer, T. The Gram Stain. Bacteriol. Rev. 1952, 16, 1–29.
  • Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G. Profiling of Complex Microbial Populations by Denaturing Gradient Gel Electrophoresis Analysis of Polymerase Chain Reaction-amplified Genes Coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59, 695–700.
  • Muyzer, G.; Brinkhoff, T.; Nübel, U.; Santegoeds, C.; Schäfer, H.; Wawer, C. Denaturing Gradient Gel Electrophoresis (DGGE) in Microbial Ecology. J. Microbiol. Methods 1998, 30, 425–468.
  • Heuer, H.; Hartung, K.; Wieland, G.; Kramer, I.; Smalla, K. Polynucleotide Probes That Target a Hypervariable Region of 16S rRNA Genes to Identify Bacterial Isolates Corresponding to Bands of Community Fingerprints. Appl. Environ. Microbiol. 1999, 65, 1045–1049.
  • Callaghan, A. V.; Davidova, I. A.; Savage-Ashlock, K.; Parisi, V. A.; Gieg, L. M.; Suflita, J. M.; Kukor, J. J.; Wawrik, B. Diversity of Benzyl- and Alkylsuccinate Synthase Genes in Hydrocarbon-impacted Environments and Enrichment Cultures. Environ. Sci. Technol. 2010, 44, 7287–7294. DOI: 10.1021/es1002023.
  • Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 2013, 30, 2725–2729. DOI: 10.1093/molbev/mst197.
  • Haines, J. R.; Wrenn, B. A.; Holder, E. L.; Strohmeier, K. L. Measurement of Hydrocarbon-degrading Microbial Populations by a 96-Well Plate Most-Probable-Number Procedure. J. Ind. Microbiol. Biotechnol. 1996, 16, 36–41. DOI: 10.1007/BF01569919.
  • Boz, D. T.; Yalcin, H. T.; Corbaci, C.; Ucar, F. B. Screening and Molecular Characterization of Polycyclic Aromatic Hydrocarbons Degrading Yeasts. Turk. Biyokim. Derg. 2015, 40, 105–110.
  • Law, A. M. J.; Aitken, M. D. Bacterial Chemotaxis to Naphthalene Desorbing from a Nonaqueous Liquid. Appl. Environ. Microbiol. 2003, 69, 5968–5973. DOI: 10.1128/AEM.69.10.5968-5973.2003.
  • Feitkenhauer, H.; Märkl, H. Biodegradation of Aliphatic and Aromatic Hydrocarbons at High Temperatures. Water Sci. Technol. 2003, 47, 123–130.
  • Bernardez, L. A.; de Andrade Lima, L. R. P.; Ramos, C. L. S.; Almeida, P. F. A Kinetic Study on Bacterial Sulfate Reduction. Mine Water Environ. 2012, 31, 62–68. DOI: 10.1007/s10230-012-0170-z.
  • Fromin, N.; Hamelin, J.; Tarnawski, S.; Roesti, D.; Jourdain-Miserez, K.; Forestier, N.; Teyssier-Cuvelle, S.; Gillet, F.; Aragono, M.; Rossi, P. Statistical Analysis of Denaturing Gel Electrophoresis (DGE) Fingerprinting Patterns. Environ. Microbiol. 2002, 4, 634–643. DOI: 10.1046/j.1462-2920.2002.00358.x.
  • Ding, A.; Sun, Y.; Dou, J.; Cheng, L.; Jiang, L.; Zhang, D.; Zhao, X. Characterizing Microbial Activity and Diversity of Hydrocarbon-Contaminated Sites. In Hydrocarbon; Kutcherov, V., Ed.; London, United Kingdom: IntechOpen, 2013; pp. 137–160.
  • Abdel-el-Haleem, D. Minireview Acinetobacter : Environmental and Biotechnological Applications. Afr. J. Biotechnol. 2003, 2, 71–74.
  • Mishra, S.; Sarma, P. M.; Lal, B. Crude Oil Degradation Efficiency of a Recombinant Acinetobacter baumannii Strain and Its Survival in Crude Oil-Contaminated Soil Microcosm. FEMS Microbiol. Lett. 2004, 235, 323–331. DOI: 10.1016/j.femsle.2004.05.002.
  • Zhang, R.; Cui, Z.; Jiang, J.; He, J.; Gu, X.; Li, S. Diversity of Organophosphorus Pesticide-Degrading Bacteria in a Polluted Soil and Conservation of Their Organophosphorus Hydrolase Genes. Can. J. Microbiol. 2005, 51, 337–343. DOI: 10.1139/w05-010.
  • Nielsen, D. R.; McLellan, P. J.; Daugulis, A. J. Direct Estimation of the Oxygen Requirements of Achromobacter xylosoxidans for Aerobic Degradation of Monoaromatic Hydrocarbons (BTEX) in a Bioscrubber. Biotechnol. Lett. 2006, 28, 1293–1298. DOI: 10.1007/s10529-006-9093-8.
  • Al-Thani, R. F.; Abd-el-Haleem, D. A. M.; Al-Shammri, M. Isolation and Characterization of Polyaromatic Hydrocarbons-Degrading Bacteria from Different Qatari Soils. Afr. J. Microbiol. Res 2009, 3, 761–766.
  • Owsianiak, M.; Szulc, A.; Chrzanowski, Ł.; Cyplik, P.; Bogacki, M.; Olejnik-Schmidt, A. K.; Heipieper, H. J. Biodegradation and Surfactant-mediated Biodegradation of Diesel Fuel by 218 Microbial Consortia Are Not Correlated to Cell Surface Hydrophobicity. Appl. Microbiol. Biotechnol. 2009, 84, 545–553. DOI: 10.1007/s00253-009-2040-6.
  • Mazzeo, D. E. C.; Levy, C. E.; de Angelis, D. D. F.; Marin-Morales, M. A. BTEX Biodegradation by Bacteria from Effluents of Petroleum Refinery. Sci. Total. Environ. 2010, 408, 4334–4340. DOI: 10.1016/j.scitotenv.2010.07.004.
  • Ugochukwu, K. C.; Agha, N. C.; Ogbulie, J. N. Lipase Activities of Microbial Isolates from Soil Contaminated with Crude Oil after Bioremediation. Afr. J. Biotechnol. 2008, 7, 2881–2884.
  • Grishchenkov, V. G.; Slepen, A. V.; Boronin, A. M. Anaerobic Degradation of Biphenyl by the Facultative Anaerobic Strain Citrobacter freundii BS2211. Appl. Biochem. Microbiol. 2002, 38, 145–148.
  • Özen, A. I.; Ussery, D. W. Defining the Pseudomonas Genus: Where Do We Draw the Line with Azotobacter?. Microb. Ecol. 2012, 63, 239–248.
  • Berney, M.; Greening, C.; Conrad, R.; Jacobs, W. R.; Cook, G. M. An Obligately Aerobic Soil Bacterium Activates Fermentative Hydrogen Production to Survive Reductive Stress During Hypoxia. Proc. Natl. Acad. Sci. USA 2014, 111, 11479–11484. DOI: 10.1073/pnas.1407034111.
  • Leuthner, B.; Heider, J. Anaerobic Toluene Catabolism of Thauera aromatica: The Bbs Operon Codes for Enzymes of β oxidation of the Intermediate Benzylsuccinate. J. Bacteriol. 2000, 182, 272–277. DOI: 10.1128/JB.182.2.272-277.2000.
  • Heider, J.; Spormann, A. M.; Beller, H. R.; Widdel, F. Anaerobic Bacterial Metabolism of Hydrocarbons. FEMS Microbiol. Rev. 1998, 22, 459–473. 1998, DOI: 10.1111/j.1574-6976.1998.tb00381.x.
  • Beller, H. R.; Spormann, A. M. Substrate Range of Benzylsuccinate Synthase from Azoarcus sp. strain T. FEMS Microbiol. Lett. 1999, 178, 147–153.
  • Widdel, F.; Rabus, R. Anaerobic Biodegradation of Saturated and Aromatic Hydrocarbons. Curr. Opin. Biotechnol. 2001, 12, 259–276.
  • Musat, F.; Galushko, A.; Jacob, J.; Widdel, F.; Kube, M.; Reinhardt, R.; Wilkes, H.; Schink, B.; Rabus, R. Anaerobic Degradation of Naphthalene and 2-methylnaphthalene by Strains of Marine Sulfate-reducing Bacteria. Environ. Microbiol 2009, 11, 209–219. DOI: 10.1111/j.1462-2920.2008.01756.x.
  • Oka, A. R.; Phelps, C. D.; Zhu, X.; Saber, D. L.; Young, L. Y. Dual Biomarkers of Anaerobic Hydrocarbon Degradation in Historically Contaminated Groundwater. Environ. Sci. Technol. 2011, 45, 3407–3414. DOI: 10.1021/es103859t.
  • Winderl, C. Functional and Phylogenetic Diversity of Anaerobic BTEX-Degrading Microorganisms in Contaminated Aquifers. Dissertation, 2007.
  • Lane, D. J. Nucleic Acids Techniques in Bacterial Systematics; Stackebrandt, E.; Goodfellow, M.; Eds.; John Wiley & Sons: Chichester, 1991; pp. 115–147.

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