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Biodegradation of naphthenic acid surrogates by axenic cultures

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Abstract

This is the first study to report that bacteria from the genera Ochrobactrum, Brevundimonas and Bacillus can be isolated by growth on naphthenic acids (NAs) extracted from oil sands process water (OSPW). These pure cultures were screened for their ability to use a range of aliphatic, cyclic and aromatic NA surrogates in 96-well microtiter plates using water-soluble tetrazolium redox dyes (Biolog Redox Dye H) as the indicator of metabolic activity. Of the three cultures, Ochrobactrum showed most metabolic activity on the widest range of NA surrogates. Brevundomonas and especially Ochrobactrum had higher metabolic activity on polycyclic aromatic compounds than other classes of NA surrogates. Bacillus also oxidized a wide range of NA surrogates but not as well as Ochrobactrum. Using this method to characterize NA utilisation, one can identify which NAs or NA classes in OSPW are more readily degraded. Since aromatic NAs have been shown to have an estrogenic effect and polycyclic monoaromatic compounds have been suggested to pose the greatest environmental threat among the NAs, these bacterial genera may play an important role in detoxification of OSPW. Furthermore, this study demonstrates that bacteria belonging to the genera Ochrobactrum and Bacillus can also degrade surrogates of tricyclic NAs.

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References

  • Alberta Environmental Protection and Enhancement Act (1993) Edmonton: Alberta Environmental Protection http://www.qp.alberta.ca/documents/Regs/1993_118.pdf

  • Allen E (2008) Process water treatment in Canada’s oil sands industry: I. Target pollutants and treatment objectives. J Environ Eng Sci 7:123–138

    Article  CAS  Google Scholar 

  • Anwar S, Liaquat F, Khan QM, Khalid ZM, Iqbal S (2009) Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1. J Hazard Mater 168:400–405

    Article  CAS  PubMed  Google Scholar 

  • Barrow MP, Headley JV, Peru KM, Derrick PJ (2004) Fourier transform ion cyclotron resonance mass spectrometry of principal components in oil sands naphthenic acids. J Chromatogr A 1058:51–59

    Article  CAS  PubMed  Google Scholar 

  • Barrow MP, Witt M, Headley JV, Peru KM (2010) Athabasca oil sands process water: characterization by atmospheric pressure photoionization and electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Anal Chem 82:3727–3735

    Article  CAS  PubMed  Google Scholar 

  • Bento FM, Camargo FAO, Okeke BC, Frankenberger WT (2005) Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresour Technol 96:1049–1055

  • Berridge MV, Herst PM, Tan AS (2005) Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Ann Rev 11:127–152

    Article  CAS  Google Scholar 

  • Biolog Technical Bulletin (2007) Biolog redox dye mixes for enumerating mammalian cells in proliferation and chemosensitivity assays. http://biolog.com/pdf/pmmlit/00P%20133rC%20Redox%20Dye%20Mix%20Brochure%20JUL07.pdf

  • Biryukova OV, Fedorak PM, Quideau SA (2007) Biodegradation of naphthenic acids by rhizosphere microorganisms. Chemosphere 67:2058–2064

    Article  CAS  PubMed  Google Scholar 

  • Blakley E (1974) The microbial degradation of cyclohexanecarboxylic acid: a pathway involving aromatization to form p-hydroxybenzoic acid. Can J Microbiol 20:1297–1306

    Article  CAS  Google Scholar 

  • Blakley E, Papish B (1982a) The metabolism of cyclohexanecarboxylic acid and 3-cyclohexenecarboxylic acid by Pseudomonas putida. Can J Microbiol 28:1324–1329

    Article  CAS  PubMed  Google Scholar 

  • Blakley ER, Papish B (1982b) The metabolism of 3-cyclohexenecarboxylic acid by Alcaligenes faecalis. Can J Microbiol 28:1037–1046

    Article  CAS  Google Scholar 

  • Brown LD, Ulrich AC (2015) Oil sands naphthenic acids: a review of properties, measurement, and treatment. Chemosphere 127:276–290

  • Calvo C, Silva-Castro G, Uad I, Fandiño CG, Laguna J, González-López J (2008) Efficiency of the EPS emulsifier produced by Ochrobactrum anthropi in different hydrocarbon bioremediation assays. J Ind Microbiol Biotechnol 35:1493–1501

    Article  CAS  PubMed  Google Scholar 

  • Chen H-J, Fan C, Lee M-S, Gong H-C, Fanchiang J-M, Tseng D-H (2010) Screening of dioxin biotransformation bacteria from the contaminated soil. In: Bioinformatics and biomedical engineering (iCBBE), 4th International conference. IEEE, pp 1–5

  • Clemente JS, Fedorak PM (2004) Evaluation of the analyses of tert-butyldimethylsilyl derivatives of naphthenic acids by gas chromatography-electron impact mass spectrometry. J Chromatogr A 1047:117–128

    Article  CAS  PubMed  Google Scholar 

  • Clemente JS, Tin-Win Y, Fedorak PM (2003) Development of a high performance liquid chromatography method to monitor the biodegradation of naphthenic acids. J Environ Eng Sci 2:177–186

    Article  CAS  Google Scholar 

  • Dan S, Li P, Stagnitti F, Xiong X (2006) Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus sp. SB02 co-immobilized on vermiculite. J Environ Sci 18:1204–1209

    Article  Google Scholar 

  • Das K, Mukherjee AK (2007) Crude petroleum-oil biodegradation efficiency of Bacillus subtilis and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from North-East India. Bioresour Technol 98:1339–1345

    Article  CAS  PubMed  Google Scholar 

  • de la Torre JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867

  • Del Rio LF, Hadwin AK, Pinto LJ, MacKinnon MD, Moore MM (2006) Degradation of naphthenic acids by sediment micro-organisms. J Appl Microbiol 101:1049–1061

  • Demeter  MA, Lemire J, George I, Yue G, Ceri H, Turner RJ (2014) Harnessing oil sands microbial communities for use in ex situ naphthenic acid bioremediation. Chemosphere 97:78–85

  • Deshpande NM, Sarnaik SS, Paranjpe SA, Kanekar PP (2004) Optimization of dimethoate degradation by Brevundimonas sp. MCM B-427 using factorial design: studies on interactive effects of environmental factors. World J Microb Biotechnol 20:455–462

    Article  CAS  Google Scholar 

  • de Vasconcellos SP, Angolini CFF, García INS, Dellagnezze BM, da Silva CC, Marsaioli AJ, dos Santos Neto EV, de Oliveira VM (2010) Screening for hydrocarbon biodegraders in a metagenomic clone library derived from Brazilian petroleum reservoirs. Org Geochem 41:675–681

  • Doddamani HP, Ninnekar HZ (2000) Biodegradation of phenanthrene by a Bacillus species. Curr Microbiol 41:11–14

    Article  CAS  PubMed  Google Scholar 

  • Dutta TK, Harayama S (2001) Biodegradation of n-alkylcycloalkanes and n-alkylbenzenes via new pathways in Alcanivorax sp strain MBIC 4326. Appl Environ Microbiol 67:1970–1974

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Feitkenhauer H, Müller R, Märkl H (2003) Degradation of polycyclic aromatic hydrocarbons and long chain alkanes at 60–70 °C by Thermus and Bacillus spp. Biodegradation 14:367–372

    Article  CAS  PubMed  Google Scholar 

  • Frank RA, Kavanagh R, Kent Burnison B, Arsenault G, Headley JV, Peru KM, Van Der Kraak G, Solomon KR (2008) Toxicity assessment of collected fractions from an extracted naphthenic acid mixture. Chemosphere 72:1309–1314

    Article  CAS  PubMed  Google Scholar 

  • Frank RA, Fischer K, Kavanagh R, Burnison BK, Arsenault G, Headley JV, Peru KM, Van Der Kraak G, Solomon KR (2009) Effect of carboxylic acid content on the acute toxicity of oil sands naphthenic acids. Environ Sci Technol 43:266–271

    Article  CAS  PubMed  Google Scholar 

  • Ghosal D, Chakraborty J, Khara P, Dutta TK (2010) Degradation of phenanthrene via meta-cleavage of 2-hydroxy-1-naphthoic acid by Ochrobactrum sp. strain PWTJD FEMS. Microbiol Lett 313:103–110

  • Giesy JP, Anderson JC, Wiseman SB (2010) Alberta oil sands development. Proc Natl Acad Sci USA 107:951–952

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Giti E, Mehdi H, Nasser G (2005) Development of a microtitre plate method for determination of phenol utilization, biofilm formation and respiratory activity by environmental bacterial isolates. Int Biodeter Biodegrad 56:231–235

    Article  CAS  Google Scholar 

  • Golby S, Ceri1 H, Gieg LM, Chatterjee I, Marques LLR, Turner RJ (2012) Evaluation of microbial biofilm communities from an Alberta oil sands tailings pond. FEMS Microbiol Ecol 79: 240–250

  • Grewer DM, Young RF, Whittal RM, Fedorak PM (2010) Naphthenic acids and other acid-extractables in water samples from Alberta: what is being measured? Sci Total Environ 408:5997–6010

    Article  CAS  PubMed  Google Scholar 

  • Grice K, Alexander R, Kagi RI (2000) Diamondoid hydrocarbon ratios as indicators of biodegradation in Australian crude oils. Org Geochem 31:67–73

    Article  CAS  Google Scholar 

  • Han XM, Scott AC, Fedorak PM, Bataineh M, Martin JW (2008) Influence of molecular structure on the biodegradability of naphthenic acids. Environ Sci Technol 42:1290–1295

    Article  CAS  PubMed  Google Scholar 

  • Hargesheimer EE, Coutts RT, MacKinnon MD (1984) Characterization of simple phenols in oil sands extraction-process water. Environ Technol 5:433–440

    Article  CAS  Google Scholar 

  • Hasegawa Y, Hamano K, Obata H, Tokuyama T (1982) Microbial degradation of cycloheptanone. Agric Biol Chem 46:1139

  • Hayes TM (2005) Examining the ecological effects of naphthenic acids and major ions on phytoplankton in the Athabasca oil sands region. Unpublished PhD Thesis, University of Waterloo, Waterloo, ON

  • He Y, Wiseman SB, Hecker M, Zhang X, Wang N, Perez LA, Jones PD, El-Din MG, Martin JW, Giesy JP (2011) Effect of ozonation on the estrogenicity and androgenicity of oil sands process-affected water. Environ Sci Technol 45:6268–6274

    Article  CAS  PubMed  Google Scholar 

  • Headley JV, Du JL, Peru KM, Gurprasad N, McMartin DW (2008) Evaluation of algal phytodegradation of petroleum naphthenic acids. J Environ Sci Health A Tox Hazard Subst Environ Eng 43:227–232

    Article  CAS  PubMed  Google Scholar 

  • Herman DC, Fedorak PM, Costerton JW (1993) Biodegradation of cycloalkane carboxylic acids in oil sand tailings. Can J Microbiol 39:576–580

    Article  CAS  PubMed  Google Scholar 

  • Herman DC, Fedorak PM, MacKinnon MD, Costerton JW (1994) Biodegradation of naphthenic acids by microbial populations indigenous to oil sands tailings. Can J Microbiol 40:467–477

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Nemati M, Hill G, Headley J (2012) Batch and continuous biodegradation of three model naphthenic acids in a circulating packed-bed bioreactor. J Hazard Mater 201:132–140

    Article  PubMed  Google Scholar 

  • Hwang G, Dong T, Islam MS, Sheng Z, Pérez-Estrada LA, Liu Y, El-Din MG (2013) The impacts of ozonation on oil sands process-affected water biodegradability and biofilm formation characteristics in bioreactors. Bioresour Technol 130:269–277

    Article  CAS  PubMed  Google Scholar 

  • Iwaki H, Nakai E, Nakamura S, Hasegawa Y (2008) Isolation and characterization of new cyclohexylacetic acid-degrading bacteria. Curr Microbiol 57:107–110

    Article  CAS  PubMed  Google Scholar 

  • Johnsen AR, Bendixen K, Karlson U (2002) Detection of microbial growth on polycyclic aromatic hydrocarbons in microtiter plates by using the respiration indicator WST-1. Appl Environ Microbiol 68:2683–2689

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson BT (2005) Microtox® acute toxicity test. In: Blaise C, Férard JF (eds) Small-scale freshwater toxicity investigations. Springer, Dordrecht, pp 69–105

    Chapter  Google Scholar 

  • Johnson RJ, Smith BE, Sutton PA, McGenity TJ, Rowland SJ, Whitby C (2011) Microbial biodegradation of aromatic alkanoic naphthenic acids is affected by the degree of alkyl side chain branching. ISME J 5:486–496

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson RJ, Smith BE, Rowland SJ, Whitby C (2013) Biodegradation of alkyl branched aromatic alkanoic naphthenic acids by Pseudomonas putida KT2440. Int Biodeter Biodegr 81:3–8

    Article  CAS  Google Scholar 

  • Johnson RJ, West CE, Swaih AM, Folwell BD, Smith BE, Rowland SJ, Whitby C (2012) Aerobic biotransformation of alkyl branched aromatic alkanoic naphthenic acids via two different pathways by a new isolate of Mycobacterium. Environ Microbiol 14:872–882

  • Jones D, Scarlett AG, West CE, Rowland SJ (2011) Toxicity of individual naphthenic acids to Vibrio fischeri. Environ Sci Technol 45:9776–9782

    Article  CAS  PubMed  Google Scholar 

  • Jones D, West CE, Scarlett AG, Frank RA, Rowland SJ (2012) Isolation and estimation of the ‘aromatic’naphthenic acid content of an oil sands process-affected water extract. J Chromatogr A 1247:171–175

    Article  CAS  PubMed  Google Scholar 

  • Kamaluddin M, Zwiazek JJ (2002) Naphthenic acids inhibit root water transport, gas exchange and leaf growth in aspen (Populus tremuloides) seedlings. Tree Physiol 22:1265–1270

    Article  CAS  PubMed  Google Scholar 

  • Kannel PR, Gan TY (2012) Naphthenic acids degradation and toxicity mitigation in tailings wastewater systems and aquatic environments: A review. J Environ Sci Health A Tox Hazard Subst Environ Engin 47:1–21

  • Kavanagh RJ, Frank RA, Oakes KD, Servos MR, Young RF, Fedorak PM, MacKinnon MD, Solomon KR, Dixon DG, Van Der Kraak G (2011) Fathead minnow (Pimephales promelas) reproduction is impaired in aged oil sands process-affected waters. Aquat Toxicol 101:214–220

    Article  CAS  PubMed  Google Scholar 

  • Lai JWS, Pinto LJ, Kiehlmann E, BendellYoung LI, Moore MM (1996) Factors that affect the degradation of naphthenic acids in oil sands wastewater by indigenous microbial communities. Environ Toxicol Chem 15:1482–1491

    Article  CAS  Google Scholar 

  • Leung SS, MacKinnon MD, Smith RE (2001) Aquatic reclamation in the Athabasca, Canada, oil sands: naphthenate and salt effects on phytoplankton communities. Environ Toxicol Chem 20:1532–1543

    Article  CAS  PubMed  Google Scholar 

  • Lister A, Nero V, Farwell A, Dixon D, Van Der Kraak G (2008) Reproductive and stress hormone levels in goldfish (Carassius auratus) exposed to oil sands process-affected water. Aquat Toxicol 87:170–177

    Article  CAS  PubMed  Google Scholar 

  • Liz JAZE, Jan-Roblero J, de la Serna JZD, de León AVP, Hernández-Rodríguez C (2009) Degradation of polychlorinated biphenyl (PCB) by a consortium obtained from a contaminated soil composed of Brevibacterium, Pandoraea and Ochrobactrum. World J Microbiol Biotechnol 25:165–170

    Article  CAS  Google Scholar 

  • MacKinnon M, Boerger H (1986) Description of two treatment methods for detoxifying oil sands tailings pond water. Water Qual Res J Can 21:496–512

    CAS  Google Scholar 

  • Mandal K, Singh B, Jariyal M, Gupta VK (2013) Microbial degradation of fipronil by Bacillus thuringiensis. Ecotox Environ Safe 93:87–92

  • Martin JW, Han XM, Peru KM, Headley JV (2008) Comparison of high- and low-resolution electrospray ionization mass spectrometry for the analysis of naphthenic acid mixtures in oil sands process water. Rapid Commun Mass Spectrom 22:1919–1924

    Article  CAS  PubMed  Google Scholar 

  • McCluskey C, Quinn JP, McGrath JW (2005) An evaluation of three new-generation tetrazolium salts for the measurement of respiratory activity in activated sludge microorganisms. Microbial Ecol 49:379–387

  • McKenzie N, Yue S, Liu X, Ramsay BA, Ramsay JA (2014) Biodegradation of naphthenic acids in oils sands process waters in an immobilized soil/sediment bioreactor. Chemosphere 109:164–172

    Article  CAS  PubMed  Google Scholar 

  • Mehdi H, Giti E (2008) Investigation of alkane biodegradation using the microtiter plate method and correlation between biofilm formation, biosurfactant production and crude oil biodegradation. Int Biodeterior Biodegrad 62:170–178

  • Misiti T, Tezel U, Pavlostathis SG (2013) Fate and effect of naphthenic acids on oil refinery activated sludge wastewater treatment systems. Water Res 47:449–460

    Article  CAS  PubMed  Google Scholar 

  • Nero V, Farwell A, Lee LEJ, Van Meer T, MacKinnon MD, Dixon DG (2006a) The effects of salinity on naphthenic acid toxicity to yellow perch: gill and liver histopathology. Ecotox Environ Safe 65:252–264

  • Nero V, Farwell A, Lister A, Van der Kraak G, Lee LE, Van Meer T, MacKinnon MD, Dixon DG (2006b) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water. Ecotoxicol Environ Saf 63:365–377

    Article  CAS  PubMed  Google Scholar 

  • Ougham H, Trudgill P (1982) Metabolism of cyclohexaneacetic acid and cyclohexanebutyric acid by Arthrobacter sp. strain CA1. J Bacteriol 150:1172–1182

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paslawski JC, Headley JV, Hill GA, Nemati M (2009) Biodegradation kinetics of trans-4-methyl-1-cyclohexane carboxylic acid. Biodegradation 20:125–133

    Article  CAS  PubMed  Google Scholar 

  • Pham TTH, Tyagi RD, Brar SK, Surampalli RY (2011) Effect of ultrasonication and Fenton oxidation on biodegradation of bis(2-ethylhexyl) phthalate (DEHP) in wastewater sludge. Chemosphere 82:923–928

    Article  CAS  PubMed  Google Scholar 

  • Quagraine EK, Headley JV, Peterson HG (2005) Is biodegradation of bitumen a source of recalcitrant naphthenic acid mixtures in oil sands tailing pond waters? J Environ Sci Health A 40:671–684

  • Quan CS, Liu Q, Tian WJ, Kikuchi J, Fan SD (2005) Biodegradation of an endocrine-disrupting chemical, di-2-ethylhexyl phthalate, by Bacillus subtilis No. 66. Appl Microbiol Biotechnol 66:702–710

    Article  CAS  PubMed  Google Scholar 

  • Quesnel DM, Bhaskar IM, Gieg LM, Chua G (2011) Naphthenic acid biodegradation by the unicellular alga Dunaliella tertiolecta. Chemosphere 84:504–511

    Article  CAS  PubMed  Google Scholar 

  • Reemtsma T, Fiehn O, Jekel M (1999) A modified method for the analysis of organics in industrial wastewater as directed by their toxicity to Vibrio fischeri Fresen. J Anal Chem 363:771–776

    Article  CAS  Google Scholar 

  • Reinardy HC, Scarlett AG, Henry TB, West CE, Hewitt LM, Frank RA, Rowland SJ (2013) Aromatic naphthenic acids in oil sands process-affected water, resolved by GCxGC-MS, only weakly induce the gene for vitellogenin production in zebrafish (Danio rerio) larvae. Environ Sci Technol 47:6614–6620

    CAS  PubMed  Google Scholar 

  • Rho E, Evans W (1975) The aerobic metabolism of cyclohexanecarboxylic acid by Acinetobacter anitratum. Biochemical J 148:11–15

  • Roehm NW, Rodgers GH, Hatfield SM, Glasebrook AL (1991) An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. J lmmunol Method 142:257–265

    Article  CAS  Google Scholar 

  • Rogers VV, Liber K, MacKinnon MD (2002) Isolation and characterization of naphthenic acids from Athabasca oil sands tailings pond water. Chemosphere 48:519–527

    Article  CAS  PubMed  Google Scholar 

  • Rogers V, MacKinnon M, Brownlee B (2007) Analytical approaches to characterising fish tainting potential of oil sands process waters. Water Sci Technol 55:311–318

    Article  CAS  PubMed  Google Scholar 

  • Rowland SJ, Scarlett AG, Jones D, West CE, Frank RA (2011a) Diamonds in the rough: identification of individual naphthenic acids in oil sands process water. Environ Sci Technol 45:3154–3159

    Article  CAS  PubMed  Google Scholar 

  • Rowland SJ, West CE, Jones D, Scarlett AG, Frank RA, Hewitt LM (2011b) Steroidal aromatic ‘naphthenic acids’ in oil sands process-affected water: structural comparisons with environmental estrogens. Environ Sci Technol 45:9806–9815

    Article  CAS  PubMed  Google Scholar 

  • Rowland SJ, West CE, Scarlett AG, Jones D, Boberek M, Pan L, Ng M, Kwong L, Tonkin A (2011c) Monocyclic and monoaromatic naphthenic acids: synthesis and characterisation. Environ Chem Lett 9:525–533

    Article  CAS  Google Scholar 

  • Rowland SJ, West CE, Scarlett AG, Jones D, Frank RA (2011d) Identification of individual tetra- and pentacyclic naphthenic acids in oil sands process water by comprehensive two-dimensional gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 25:1198–1204

    Article  CAS  PubMed  Google Scholar 

  • Scarlett AG, West CE, Jones D, Galloway TS, Rowland SJ (2012) Predicted toxicity of naphthenic acids present in oil sands process-affected waters to a range of environmental and human endpoints. Sci Total Environ 425:119–127

    Article  CAS  PubMed  Google Scholar 

  • Scott AC, MacKinnon MD, Fedorak PM (2005) Naphthenic acids in athabasca oil sands tailings waters are less biodegradable than commercial naphthenic acids. Environ Sci Technol 39:8388–8394

    Article  CAS  PubMed  Google Scholar 

  • Scudiero DA, Shoemaker RH, Paull KD, Monks A, Tierney S, Nofziger TH, Currens MJ, Seniff D, Boyd MR (1988) Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res 48:4827–4833

    CAS  PubMed  Google Scholar 

  • Selifonov SA (1992) Microbial oxidation of adamantanone by Pseudomonas putida carrying the camphor catabolic plasmid. Biochem Biophys Res Comm 186:1429–1436

    Article  CAS  PubMed  Google Scholar 

  • Siwik PL, Van Meer T, MacKinnon MD, Paszkowski CA (2000) Growth of fathead minnows in oilsand-processed wastewater in laboratory and field. Environ Toxicol Chem 19:1837–1845

    Article  CAS  Google Scholar 

  • Smith BE, Lewis CA, Belt ST, Whitby C, Rowland SJ (2008) Effects of alkyl chain branching on the biotransformation of naphthenic acids. Environ Sci Technol 42:9323–9328

    Article  CAS  PubMed  Google Scholar 

  • Sonke T, Ernste S, Tandler RF, Kaptein B, Peeters WP, van Assema FB, Wubbolts MG, Schoemaker HE (2005) L-selective amidase with extremely broad substrate specificity from Ochrobactrum anthropi NCIMB 40321. Appl Environ Microbiol 71:7961–7973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Strong-Gunderson JM, Palumbo AV (1994) Alternative method for rapidly screening microbial isolates for their potential to degrade volatile contaminants. J Ind Microbiol 13:361–366

    Article  CAS  PubMed  Google Scholar 

  • Sylvester PW (2011) Optimization of the tetrazolium dye (MTT) colorimetric assay for cellular growth and viability. In: Satyanarayanajois SD (ed) Drug design and discovery methods and protocols. Methods in molecular biology. Humana Press, New York, pp 157–168

    Chapter  Google Scholar 

  • Toor NS, Franz ED, Fedorak PM, MacKinnon MD, Liber K (2013) Degradation and aquatic toxicity of naphthenic acids in oil sands process-affected waters using simulated wetlands. Chemosphere 90:449–458

  • Videla P, Farwell A, Butler B, Dixon DG (2009) Examining the microbial degradation of naphthenic acids using stable isotope analysis of carbon and nitrogen. Water Air Soil Pollut 197:107–119

    Article  CAS  Google Scholar 

  • Wei Z, Moldowan JM, Peters KE, Wang Y, Xiang W (2007) The abundance and distribution of diamondoids in biodegraded oils from the San Joaquin Valley: implications for biodegradation of diamondoids in petroleum reservoirs. Org Geochem 38:1910–1926

    Article  CAS  Google Scholar 

  • Whitby C (2010) Microbial naphthenic acid degradation. Adv Appl Microbiol 70:93–125

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Guo L, Wang S, Lu Y (2010) Comparative impact of cadmium on two phenanthrene-degrading bacteria isolated from cadmium and phenanthrene co-contaminated soil in China. J Hazard Mater 174:818–823

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Institute for Oils and Innovation at the University of Alberta (IOSI).

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  1. Chemical Engineering, Queen’s University, Kingston, ON, K7L 3N6, Canada

    Siqing Yue, Bruce A. Ramsay & Juliana A. Ramsay

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Yue, S., Ramsay, B.A. & Ramsay, J.A. Biodegradation of naphthenic acid surrogates by axenic cultures. Biodegradation 26, 313–325 (2015). https://doi.org/10.1007/s10532-015-9736-3

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