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Aerobic biodegradation of organic compounds in hydraulic fracturing fluids

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Abstract

Little is known of the attenuation of chemical mixtures created for hydraulic fracturing within the natural environment. A synthetic hydraulic fracturing fluid was developed from disclosed industry formulas and produced for laboratory experiments using commercial additives in use by Marcellus shale field crews. The experiments employed an internationally accepted standard method (OECD 301A) to evaluate aerobic biodegradation potential of the fluid mixture by monitoring the removal of dissolved organic carbon (DOC) from an aqueous solution by activated sludge and lake water microbial consortia for two substrate concentrations and four salinities. Microbial degradation removed from 57 % to more than 90 % of added DOC within 6.5 days, with higher removal efficiency at more dilute concentrations and little difference in overall removal extent between sludge and lake microbe treatments. The alcohols isopropanol and octanol were degraded to levels below detection limits while the solvent acetone accumulated in biological treatments through time. Salinity concentrations of 40 g/L or more completely inhibited degradation during the first 6.5 days of incubation with the synthetic hydraulic fracturing fluid even though communities were pre-acclimated to salt. Initially diverse microbial communities became dominated by 16S rRNA sequences affiliated with Pseudomonas and other Pseudomonadaceae after incubation with the synthetic fracturing fluid, taxa which may be involved in acetone production. These data expand our understanding of constraints on the biodegradation potential of organic compounds in hydraulic fracturing fluids under aerobic conditions in the event that they are accidentally released to surface waters and shallow soils.

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References

  • Abualfaraj N, Gurian P, Olson M (2014) Characterization of Marcellus Shale flowback water. Environ Eng Sci 31(9):514–524

    Article  CAS  Google Scholar 

  • Adroer N, Casas C, Mas C, Solá C (1990) Mechanism of formaldehyde biodegradation by Pseudomonas putida. Appl Microbiol Biotechnol 33(2):217–220

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Arthur J, Bohm B, Layne M (2008) Hydraulic fracturing considerations for natural gas wells of the Marcellus Shale. In: Paper presented at the The Ground Water Protection Council Annual Forum, Cincinatti, OH

  • Arvin E, Jensen BK, Gundersen AT (1989) Substrate interactions during aerobic biodegradation of benzene. Appl Environ Microbiol 55(12):3221–3225

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aukema KG, Kasinkas L, Aksan A, Wackett LP (2014) Biodegradation of novel hydrocarbon ring structures found in hydraulic fracturing waters using silica-encapsulated pseudomonas sp. NCIB 9816-4. Appl Environ Microbiol 80(16):4968–4976

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barathi S, Vasudevan N (2001) Utilization of petroleum hydrocarbons by Pseudomonas fluorescens isolated from a petroleum-contaminated soil. Environ Int 26(5–6):413–416

    Article  CAS  PubMed  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5(5):908–917

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beal R, Betts WB (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89(1):158–168

    Article  CAS  PubMed  Google Scholar 

  • Bielefeldt AR, Stensel HD (1999) Modeling competitive inhibition effects during biodegradation of BTEX mixtures. Water Res 33(3):707–714

    Article  CAS  Google Scholar 

  • Bosch R, Garcia-Valdes E, Moore ERB (2000) Complete nucleotide sequence and evolutionary significance of a chromosomally encoded naphthalene-degradation lower pathway from Pseudomonas stutzeri AN10. Gene 245(1):65–74

    Article  CAS  PubMed  Google Scholar 

  • Bouchez M, Blanchet D, Vandecasteele JP (1995) Degradation of polycyclic aromatic hydrocarbons by pure strains and by defined strain associations: inhibition phenomena and cometabolism. Appl Microbiol Biotechnol 43(1):156–164

    Article  CAS  PubMed  Google Scholar 

  • Brantley SL, Yoxtheimer D, Arjmand S, Grieve P, Vidic R, Pollak J, Llewellyn GT, Abad J, Simon C (2014) Water resource impacts during unconventional shale gas development: the Pennsylvania experience. Int J Coal Geol 126:140–156

    Article  CAS  Google Scholar 

  • Bustard MT, McEvoy EM, Goodwin JAS, Burgess JG, Wright PC (2000) Biodegradation of propanol and isopropanol by a mixed microbial consortium. Appl Microbiol Biotechnol 54(3):424–431

    Article  CAS  PubMed  Google Scholar 

  • Bustard M, Whiting S, Cowan D, Wright P (2002) Biodegradation of high-concentration isopropanol by a solvent-tolerant thermophile, Bacillus pallidus. Extremophiles 6(4):319–323

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cluff MA, Hartsock A, MacRae JD, Carter K, Mouser PJ (2014) Temporal changes in microbial ecology and geochemistry in produced water from hydraulically fractured Marcellus Shale gas wells. Environ Sci Technol 48(11):6508–6517

    Article  CAS  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Evans WH, David EJ (1974) Biodegradation of mono-. di- and triethylene glycols in river waters under controlled laboratory conditions. Water Res 8(2):97–100

    Article  CAS  Google Scholar 

  • Filonov AE, Karpov AV, Kosheleva IA, Puntus IF, Balashova NV, Boronin AM (2000) The efficiency of salicylate utilization by Pseudomonas putida strains catabolizing naphthalene via different biochemical pathways. Process Biochem 35(9):983–987

    Article  CAS  Google Scholar 

  • Frossard A, Gerull L, Mutz M, Gessner MO (2013) Shifts in microbial community structure and function in stream sediments during experimentally simulated riparian succession. FEMS Microbiol Ecol 84(2):398–410

    Article  CAS  PubMed  Google Scholar 

  • Gai Z, Zhang Z, Wang X, Tao F, Tang H, Xu P (2012) Genome sequence of Pseudomonas aeruginosa DQ8, an efficient degrader of n-alkanes and polycyclic aromatic hydrocarbons. J Bacteriol 194(22):6304–6305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gebeloff R, Sontag D (2014) The downside of the boom. NY Times, 22 November 2014

  • Gregory KB, Vidic RD, Dzombak DA (2011) Water management challenges associated with the production of shale gas by hydraulic fracturing. Elements 7(3):181–186

    Article  Google Scholar 

  • Guha S, Peters CA, Jaffé PR (1999) Multisubstrate biodegradation kinetics of naphthalene, phenanthrene, and pyrene mixtures. Biotechnol Bioeng 65(5):491–499

    Article  CAS  PubMed  Google Scholar 

  • Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, The Human Microbiome C, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21(3):494–504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayes T (2009) Sampling and analysis of water streams associated with the development of Marcellus Shale gas. Report by Gas Technology Institute, Des Plaines, for the Marcellus Shale Coalition

  • Jiang M, Hendrickson CT, VanBriesen JM (2013) Life cycle water consumption and wastewater generation impacts of a Marcellus Shale gas well. Environ Sci Technol 48(3):1911–1920

    Article  PubMed Central  Google Scholar 

  • Jones DT, Woods DR (1986) Acetone-butanol fermentation revisited. Microbiol Rev 50(4):484

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kaczorek E, Moszyńska S, Olszanowski A (2011) Modification of cell surface properties of Pseudomonas alcaligenes S22 during hydrocarbon biodegradation. Biodegradation 22(2):359–366

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kahrilas GA, Blotevogel J, Stewart P, Borch T (2015) Biocides in hydraulic fracturing fluids: a critical review of their usage, mobility, degradation, and toxicity. Environ Sci Technol 49(1):16–32

    Article  CAS  PubMed  Google Scholar 

  • King GE Hydraulic Fracturing 101: What every representative environmentalist regulator reporter investor university researcher neighbor and engineer should know about estimating frac risk and improving frac performance in unconventional gas and oil wells, SPE 152596. In: SPE hydraulic fracturing technology conference, Woodlands, TX, 6–8 February 2012. Society of Petroleum Engineers, pp 1–80

  • Klecka GM, Carpenter CL, Landenberger BD (1993) Biodegradation of aircraft deicing fluids in soil at low temperatures. Ecotoxicol Environ Saf 25(3):280–295

    Article  CAS  PubMed  Google Scholar 

  • Kotani T, Yurimoto H, Kato N, Sakai Y (2007) Novel acetone metabolism in a propane-utilizing bacterium, Gordonia sp. Strain TY-5. J Bacteriol 189(3):886–893

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lefebvre O, Moletta R (2006) Treatment of organic pollution in industrial saline wastewater: a literature review. Water Res 40(20):3671–3682

    Article  CAS  PubMed  Google Scholar 

  • Lester Y, Yacob T, Morrissey I, Linden KG (2014) Can we treat hydraulic fracturing flowback with a conventional biological process? the case of guar gum. Environ Sci Technol Lett 1(1):133–136

    Article  CAS  Google Scholar 

  • Leung H-W (2001) Ecotoxicology of glutaraldehyde: review of environmental fate and effects studies. Ecotoxicol Environ Saf 49(1):26–39

    Article  CAS  PubMed  Google Scholar 

  • Levin I, Meiri G, Peretz M, Burstein Y, Frolow F (2004) The ternary complex of Pseudomonas aeruginosa alcohol dehydrogenase with NADH and ethylene glycol. Protein Sci 13(6):1547–1556

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li B, Zhang X, Guo F, Wu W, Zhang T (2013) Characterization of tetracycline resistant bacterial community in saline activated sludge using batch stress incubation with high-throughput sequencing analysis. Water Res 47(13):4207–4216

    Article  CAS  PubMed  Google Scholar 

  • Littlejohns JV, Daugulis AJ (2008) Kinetics and interactions of BTEX compounds during degradation by a bacterial consortium. Process Biochem 43(10):1068–1076

    Article  CAS  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mauter M, Palmer V (2014) Expert elicitation of trends in Marcellus oil and gas wastewater management. J Environ Eng 140(Environmental Impacts of Shale Gas Development, B4014004):1–9

    Google Scholar 

  • Mohan A, Hartsock A, Bibby KJ, Hammack RW, Vidic RD, Gregory KB (2013a) Microbial community changes in hydraulic fracturing fluids and produced water from shale gas extraction. Environ Sci Technol 47(22):13141–13150

    Article  Google Scholar 

  • Mohan AM, Hartsock A, Hammack R, Vidic RD, Gregory KB (2013b) Microbial communities in flowback water impoundments from hydraulic fracturing for recovery of shale gas. FEMS Microbiol Ecol 86(3):567–580

    Article  Google Scholar 

  • Mouser PJ, Liu S, Cluff MA, McHugh M, Lenhart JJ, MacRae JD (in review) Biodegradation of hydraulic fracturing fluid organic additives in sediment-groundwater microcosms. J Hazard Mater

  • Mrklas O, Chu A, Lunn S, Bentley L (2004) Biodegradation of monoethanolamine, ethylene glycol and triethylene glycol in laboratory bioreactors. Water Air Soil Pollut 159(1):249–263

    Article  CAS  Google Scholar 

  • Ng H, Ong S, Ng W (2005) Effects of sodium chloride on the performance of a sequencing batch reactor. J Environ Eng 131(11):1557–1564

    Article  CAS  Google Scholar 

  • Ny DEP (2011) Revised draft: supplemental generic environmental impact statement on the oil, gas and solution mining regulatory program: well permit issuance for horizontal drilling and high-volume hydraulic fracturing to develop the Marcellus Shale and other low-permeability gas reservoirs. New York Department of Environmental Protection, Albany

  • OECD (1994) Organization for Economic Cooperation and Development (OECD) guidelines for the testing of chemicals. vol Section 3: degradation and accumulation, 2nd edn. Organization for Economic Cooperation and Development. doi:10.1787/9789264070349-en

  • Orem W, Tatu C, Varonka M, Lerch H, Bates A, Engle M, Crosby L, McIntosh J (2014) Organic substances in produced and formation water from unconventional natural gas extraction in coal and shale. Int J Coal Geol 126:20–31

    Article  CAS  Google Scholar 

  • PA DEP (2014) Pennsylvania Department of Environmental Protection Oil and Gas reporting website. http://www.paoilandgasreporting.state.pa.us/publicreports/Modules/Welcome/Welcome.aspx

  • Rahm B, Bates J, Bertoia L, Galford A, Yoxtheimer D, Riha S (2013) Wastewater management and Marcellus Shale gas development: trends, drivers, and planning implications. J Environ Manage 120:105–113

    Article  PubMed  Google Scholar 

  • Ramos JL, Duque E, Huertas MJ, Haïdour A (1995) Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons. J Bacteriol 177(14):3911–3916

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reardon KF, Mosteller DC, Bull Rogers JD (2000) Biodegradation kinetics of benzene, toluene, and phenol as single and mixed substrates for Pseudomonas putida F1. Biotechnol Bioeng 69(4):385–400

    Article  CAS  PubMed  Google Scholar 

  • Reid MF, Fewson CA (1994) Molecular characterization of microbial alcohol dehydrogenases. Crit Rev Microbiol 20(1):13–56

    Article  CAS  PubMed  Google Scholar 

  • Rocha CA, Pedregosa AM, Laborda F (2011) Biosurfactant-mediated biodegradation of straight and methyl-branched alkanes by Pseudomonas aeruginosa ATCC 55925. AMB express 1(1):1–10

    Article  Google Scholar 

  • Romanenko LA, Uchino M, Falsen E, Zhukova NV, Mikhailov VV, Uchimura T (2003) Rheinheimera pacifica sp. nov., a novel halotolerant bacterium isolated from deep sea water of the Pacific. Int J Syst Evol Microbiol 53(6):1973–1977

    Article  CAS  PubMed  Google Scholar 

  • Rowan EL, Engle MA, Kraemer TF, Schroeder KT, Hammack RW, Doughten M (2014) Geochemical and isotopic evolution of water produced from Middle Devonian Marcellus Shale gas wells, Appalachian basin, Pennsylvania. AAPG Bulletin 99(2):181–206

    Article  Google Scholar 

  • Shinoda Y, Sakai Y, Uenishi H, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Kato N (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. Strain DNT-1. Appl Environ Microbiol 70(3):1385–1392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soeder DJ (2010) The Marcellus Shale: resources and reservations. EOS 91(32):277–279

    Article  Google Scholar 

  • Songa J, Zhanga L, Leeb Y, Jeongc J, Leec J, Jahnga D (2010) Evaluation of isopropyl alcohol degrading bacteria isolated from a MBR sludge. Southeast Asian Water Environ 4:121

    Google Scholar 

  • Staples CA, Williams JB, Craig GR, Roberts KM (2001) Fate, effects and potential environmental risks of ethylene glycol: a review. Chemosphere 43(3):377–383

    Article  CAS  PubMed  Google Scholar 

  • Stingl U, Tripp HJ, Giovannoni SJ (2007) Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time Series study site. ISME J 1(4):361–371

    CAS  PubMed  Google Scholar 

  • Stringfellow WT, Domen JK, Camarillo MK, Sandelin WL, Borglin S (2014) Physical, chemical, and biological characteristics of compounds used in hydraulic fracturing. J Hazard Mater 275:37–54

    Article  CAS  PubMed  Google Scholar 

  • Strong L, Gould T, Kasinkas L, Sadowsky M, Aksan A, Wackett L (2014) Biodegradation in waters from hydraulic fracturing: chemistry, microbiology, and engineering. J Environ Eng 140(5):B4013001

    Article  Google Scholar 

  • Struchtemeyer CG, Elshahed MS (2012) Bacterial communities associated with hydraulic fracturing fluids in thermogenic natural gas wells in North Central Texas, USA. FEMS Microbiol Ecol 81(1):13–25

    Article  CAS  PubMed  Google Scholar 

  • Struchtemeyer CG, Morrison MD, Elshahed MS (2012) A critical assessment of the efficacy of biocides used during the hydraulic fracturing process in shale natural gas wells. Int Biodeterior Biodegrad 71:15–21

    Article  CAS  Google Scholar 

  • Takizawa N, Kaida N, Torigoe S, Moritani T, Sawada T, Satoh S, Kiyohara H (1994) Identification and characterization of genes encoding polycyclic aromatic hydrocarbon dioxygenase and polycyclic aromatic hydrocarbon dihydrodiol dehydrogenase in Pseudomonas putida OUS82. J Bacteriol 176(8):2444–2449

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tang H, Yu H, Li Q, Wang X, Gai Z, Yin G, Su F, Tao F, Ma C, Xu P (2011) Genome sequence of Pseudomonas putida strain B6-2, a superdegrader of polycyclic aromatic hydrocarbons and dioxin-like compounds. J Bacteriol 193(23):6789–6790

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tasaki Y, Yoshikawa H, Tamura H (2006) Isolation and characterization of an alcohol dehydrogenase gene from the octylphenol polyethoxylate degrader Pseudomonas putida S-5. Biosci Biotechnol Biochem 70(8):1855–1863

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Ma P, Zhong J-J (2003) Impact of the presence of salicylate or glucose on enzyme activity and phenanthrene degradation by Pseudomonas mendocina. Process Biochem 38(8):1125–1132

    Article  CAS  Google Scholar 

  • USEPA (2010) Toxicological review of ethylene glycol monobutyl ether. Office of Research and Development, Washington, DC

    Google Scholar 

  • USEPA (2012) Study of the potential impacts of hydraulic fracturing on drinking water resources: progress report. Office of Research and Development, Washington, DC

    Google Scholar 

  • Vidic RD, Brantley SL, Vandenbossche JM, Yoxtheimer D, Abad JD (2013) Impact of shale gas development on regional water quality. Science 340(6134):1235009

    Article  CAS  PubMed  Google Scholar 

  • Vikram A, Lipus D, Bibby K (2014) Produced water exposure alters bacterial response to biocides. Environ Sci Technol 48(21):13001–13009

    Article  CAS  PubMed  Google Scholar 

  • Waxman H, Markey E, DeGette D (2011) Chemicals used in hydraulic fracturing. U.S. House of Representatives, Committee on Energy and Commerce

  • Weissbrodt DG, Shani N, Holliger C (2014) Linking bacterial population dynamics and nutrient removal in the granular sludge biofilm ecosystem engineered for wastewater treatment. FEMS Microbiol Ecol 88(3):579–595

    Article  CAS  PubMed  Google Scholar 

  • Whyte LG, Bourbonniére L, Greer CW (1997) Biodegradation of petroleum hydrocarbons by psychrotrophic Pseudomonas strains possessing both alkane (alk) and naphthalene (nah) catabolic pathways. Appl Environ Microbiol 63(9):3719–3723

    CAS  PubMed Central  PubMed  Google Scholar 

  • Williams PA, Sayers JR (1994) The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas. Biodegradation 5(3–4):195–217

    Article  CAS  PubMed  Google Scholar 

  • Woods J (2014) Fish kill in eastern Ohio might be linked to fire at fracking well. Columbus Dispatch, 30 June 2014

  • Yeo CC, Wong MV-M, Feng Y, Song KP, Poh CL (2003) Molecular characterization of an inducible gentisate 1,2-dioxygenase gene, xlnE, from Pseudomonas alcaligenes NCIMB 9867. Gene 312:239–248

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Xu D, Zhu C, Lundaa T, Scherr KE (2012) Isolation and identification of biosurfactant producing and crude oil degrading Pseudomonas aeruginosa strains. Chem Eng J 209:138–146

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by NSF CBET Award #1247338 to P.J.M and NSF CBET Award #1336326 to P.J.M and D.P. We are grateful for donations of chemical additives from the manufacturers for our synthetic fracturing fluid. We greatly appreciate assistance from Michael Wilkins and Michael Johnson for cell counting and thank Alum Creek Wastewater Treatment Facility for providing activated sludge.

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Kekacs, D., Drollette, B.D., Brooker, M. et al. Aerobic biodegradation of organic compounds in hydraulic fracturing fluids. Biodegradation 26, 271–287 (2015). https://doi.org/10.1007/s10532-015-9733-6

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