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In this work, we explored the potential for growth of a unicellular algae, Chlorella pyrenoidosa, in tailings water from an oil sands mining and upgra...
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Potential for CO2 Fixation by Chlorella pyrenoidosa Grown in Oil Sands Tailings Water Swati Yewalkar, Belinda Li, Dusko Posarac, and Sheldon Duff* Department of Chemical and Biological Engineering, University of British Columbia, 2360 East Mall, Vancouver, British Columbia, V6T 1Z3, Canada ABSTRACT: Discharge of process water into tailings ponds is associated with many mining operations, including that of bitumen. These tailings ponds can be used to grow organisms, such as algae, which, in turn, fix CO2 and degrade unwanted dissolved components. After processing, algae can be used for the production of fuels (for example, biodiesel or methane). In this work, we explored the potential for growth of a unicellular algae, Chlorella pyrenoidosa, in tailings water from an oil sands mining and upgrading operation. Once we determined that it was possible to grow algae in the tailings water, we designed and optimized minimal growth media for biomass (algae) production and did a preliminary engineering estimate of the potential for CO2 fixation. The medium components required for growth of C. pyrenoidosa in 95% oil sands tailings water (OSTW) were screened using a twolevel full factorial experiment. Sodium nitrate, phosphate, and Fe-ethylenediaminetetraacetic acid (EDTA) were the most important medium components. After this work, response surface methodology (RSM) was used to find the optimum concentrations of these nutrients. The optimum concentrations of sodium nitrate, phosphate, Fe-EDTA, and trace metal solution were 11.9 mM, 9.4 mM, 49.5 μM, and 2 mL/L, respectively. On the basis of an optimized specific growth rate of 0.085 g L1 day1, it was estimated that 12 million tons/year of CO2 could be fixed by C. pyrenoidosa growing in the tailings ponds in the Athabasca region of Canada. This value has to be considered optimistic because of fluctuations in temperature, light, and other growing conditions, which would be experienced in the full-scale system.

’ INTRODUCTION The Athabasca oil sands deposits in northern Alberta, Canada, are the largest source of oil sands in the world. The oil industry in this region has rapidly expanded its capacity to produce crude oil from oil sands, nearly doubling production from 0.66 million barrels per day (bbl/d) in 2001 to 1.2 million bbl/d in 2007.1 The methods used for extraction of bitumen and generation of oil sands tailings water (OSTW) are described in the literature.2,3 There exists considerable incentive to develop technologies for beneficial use of these tailings ponds. OSTW contains a wide range of chemicals, which have been primarily studied because of their potential toxic effects on receiving waters.410 However, OSTW contains some macro- and micronutrients, making it potentially suitable for growth of microorganisms (Table 1). Headley et al. reported growth of 12 algae from different classes in the naphthenic acid extracted from oil sands tailings water and in surrogate naphthenic acid.11 Further, growth of several genera of algae, including Botryococcus braunii, Chlamydomonas, Cryptomonas, Ochromonas, Chromulina, Oscillatoria, Navicula, and Nitzschia have been observed in tailings ponds.12 It is well-known that supplementation of natural water bodies with nutrients, such as phosphates, nitrates, and ferrous ions, enhance phytoplankton growth1315 and can stimulate the degradation of complex petroleum products,16,17 even in OSTW.18 The fossil fuel industry is one of the largest and most concentrated sources of greenhouse gases in Canada. In 2004, the fossil fuel industry contributed 155 megatons of CO2 equivalent of greenhouse gas emissions, which was 20% of the national total.19 Oil sands operations in Alberta are one of the largest emitters of CO2 in the oil industry, because of the energy demand r 2011 American Chemical Society

associated with processing bitumen. Growth of autotrophs, such as algae, is one proposed method for fixing atmospheric CO2. Chlorella sp. is one of the most commonly used genera of algae for CO2 fixation because of their productivity and resilience. Murakami and Ikenouchi screened and bred more than 10 strains of algae that were considered to have good rates of CO2 fixation.20 Chlorella sp. had a CO2 fixation rate of at least 1 g of CO2 L1 day1 when grown in small-scale cultures. de Morais and Costa collected water samples from a coal-fired thermoelectric plant to find algae that would be tolerant to the conditions prevalent near the plant.21 Chlorella kessleri was one of the most dominant species recovered from the water samples. The oil sands industry in Alberta uses approximately 349 million m3 of water each year, of which at least 90% is sent to tailings ponds as hot water extraction plumes.22 Hot water extraction slurry has an average temperature from 35 to 80 °C, depending upon the process used. Spanning more than 50 km2, the water and waste heat from tailings ponds provide a potential environment for algae to live and capture CO2 from the oil sands operations. This paper was aimed at an initial assessment of the technical feasibility of growing algae in tailings water from an oil sands processing facility in Alberta. Specifically, the objectives were to select a species of algae that could grow in tailings water, develop a low-cost defined medium for its growth, determine growth kinetics using the optimized medium, and carry out a preliminary estimate of the potential for CO2 fixation via this route. Received: November 5, 2010 Revised: February 25, 2011 Published: March 04, 2011 1900

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’ MATERIALS AND METHODS

0.67 mM KCl, 0.5 mM NH4Cl, 15 μM Na2EDTA, 2.15 μM FeCl3 3 6 H2O, 1.24 μM MnCl2 3 4H2O, 0.22 μM ZnSO4, 0.05 μM CoCl2 3 6H2O, 0.12 μM NH3MoO4 3 2H2O, 0.000 11 μM vitamin B12, and 0.001 μM biotin. The pH of the growth medium was adjusted to 6.7 using 1 N NaOH. Aliquots (125 mL) of growth medium were added to each of four 250 mL Erlenmeyer flasks. The flasks were then topped with foam plugs and autoclaved on the liquid cycle at 121 °C for 20 min. For experiments that examined the impact of tailings concentration, the same medium was prepared at double-strength and mixed with various volumes of filter-sterilized tailings water to give medium with a final volumetric concentration of tailings water of 0, 10, 30, and 50% (v/v). The MES-Volvox medium used in the initial trial is a complex medium containing a number of expensive components, including an organic carbon source. Efforts were undertaken to develop a more practical medium to support the growth of C. pyrenoidosa in 95% OSTW. This was accomplished by first formulating a defined medium based on a survey of published literature. Based on this review, the defined growth medium initially devised consisted of 1.83 mM Na2HPO4, 5.58 mM KH2PO4, 11.76 mM NaNO3, 0.068 mM CaCl2, 0.20 mM MgSO4, 47.01 μM Feethylenediaminetetraacetic acid (EDTA), 0.083 μM ZnSO4, 0.084 μM CoCl2, 0.032 μM (NH4)6Mo7O24 3 3H2O, 0.01 μM vitamin B12, 0.36 μM thiamine, and 0.01 μM biotin. Following this, a two-stage experimental plan was used to optimize the growth medium. First, a full factorial design (Table 2) was used to determine the relative importance of several media components. A second central composite design (Table 3) was undertaken to determine the optimal concentrations of each tested component. Growth Conditions. All growth trials were conducted under static conditions at room temperature (approximately 25 °C) and ambient atmospheric conditions. The flasks were continuously illuminated using full spectrum grow lights on a stand 20 cm above the surface of the flasks. Under these conditions, the light intensity was 125 μmol m2 s1 (Fieldscout quantum light meter, Spectrum Technology, Plainfield, IL). Measurement of the Algal Growth Rate. Growth of C. pyrenoidosa was assessed using two different methods. For the initial study aimed at determining whether the OSTW would inhibit algal growth, the biomass concentration was estimated using optical density. For subsequent experiments, the algae concentration was determined by direct cell counts using a hemocytometer (Fisher Scientific, Waltham,

Algae Stock. The algae used for this study was Chlorella pyrenoidosa CCCM 7066 obtained from the Canadian Centre for Culture of Microorganisms (CCCM) at the University of British Columbia (UBC). The algae stock was obtained in four 50 mL Falcon tubes. They were stored in at 4 °C with the screw caps loosened to allow for aeration. Tailings Preparation. A sample of tailings pond water was obtained from an oil sands upgrading operation in northern Alberta. The tailings were high in suspended solids, which would interfere with the measurement of dry biomass concentration through optical density. Because of this, approximately 1 L of the sample was divided equally into 50 mL Falcon tubes and centrifuged in an IEC CU-3000 centrifuge at a g force of 3600 for 30 min. The supernatant was retained and filtersterilized through a 0.22 μm filter into a sterile 1 L Nalgene bottle for storage. Growth Medium. The growth medium used for C. pyrenoidosa was MES-Volvox. The composition of this medium is 0.5 mM Ca(NO3)2 3 4 H2O, 0.16 mM MgSO4 3 7H2O, 0.2 mM Na-β-glycerophosphate 3 5H2O,

Table 1. Typical Values for Nutrients Available for Algal Growth in OSTW3,8 nutrients present

concentration (mg/L)

macronutrients NH3

6823.9

PO43

0.020.4

HCO3

10001137

micronutrients Naþ

410870

Mgþ Caþ

310 614

Feþ

0.080.9

Mn

0.0040.026

Mo

0.183

Ni

0.0010.014

Table 2. Full Factorial Design with Coded and Actual Level of Variables sodium nitrate (X1)

phosphate (X2)

experiment number

coded level

actual level (mM)

coded level

1 2

þ1 þ1

11.76 11.76

1 1

3

1

4

þ1

0 11.76

actual level (mM) 0 0

FeEDTA (X3)

trace metal solution (X4)

coded level

actual level (μM)

coded level

actual level (mL/L)

þ1 1

47 0

1 1

0 0

1

0

þ1

47

þ1

2

þ1

7.6

1

0

1

0

5

1

0

1

0

þ1

47

1

0

6

1

0

þ1

7.6

1

0

1

0

7

1

0

1

0

1

0

þ1

2

8

1

0

þ1

7.6

þ1

47

1

0

9 10

1 þ1

þ1 þ1

7.6 7.6

1 1

0 0

þ1 þ1

2 2

11

1

þ1

7.6

þ1

47

þ1

2

12

þ1

1

0

1

0

þ1

2

0 11.76 0 11.76

13

þ1

11.76

1

0

þ1

47

þ1

2

14

þ1

11.76

þ1

7.6

þ1

47

1

0

15

1

16

þ1

0 11.76

1

0

1

0

1

0

þ1

7.6

þ1

47

þ1

2

1901

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Table 3. Central Composite Experimental (Uniform Precision) Design for Optimizing the Concentration of Nitrate, Phosphate FeEDTA, and Trace Metals sodium nitrate (X1) experiment number

coded

phosphate (X2)

FeEDTA (X3)

actual (mM)

coded

actual (mM)

coded

actual (μM)

trace metal solution (X4) coded

actual (mL/L)

1

0

11.4



0.84

0

47

0

2

2



6



3.7

þ

70

þ

3

3 4

þ 0

16.8 11.4

þ 0

11.1 7.4

þ δ

70 6.3

 0

1 2

5



6



3.7

þ

70



1

6

þ

16.8

þ

11.1



24

þ

3

7

þδ

20.96

0

7.4

0

47

0

2

8

0

11.4

0

7.4

0

47

0

2

9



1.8

0

7.4

0

47

0

2

10



6

þ

11.1



24



1

11 12

 þ

6 16.8

þ 

11.1 3.7

þ þ

70 70

þ 

3 1

13



6



3.7



24



1

14



6

þ

11.1

þ

70



1

15

0

11.4

0

7.4

0

47

0

2

16

0

11.4

0

7.4

0

47

0

2

17

0

11.4

0

7.4

0

47

0

2

18

þ

16.8



3.7



24



1

19 20

þ 0

16.8 11.4

þ 0

11.1 7.4

 0

24 47

 0

1 2

21

þ

16.8



3.7

þ

70

þ

3

22

0

11.4

þδ

13.95

0

47

0

2

23

0

11.4

0

7.4

þδ

87.7

0

2

24

0

11.4

0

7.4

0

47

0

2

25

þ

16.8

þ

11.1

þ

70

þ

3

26



6

þ

11.1



24

þ

3

27 28

 0

6 11.4

 0

3.7 7.4

 0

24 47

þ þδ

3 3.77

29

0

11.4

0

7.4

0

47

0

2

30

þ

16.8



3.7



24

þ

3

31

0

11.4

0

7.4

0

47



0.229

MA) under a light microscope (Olympus, Japan). The number of algae cells at each condition was a mean of three counts. The specific growth rate (SGR) was calculated using the method published by Sung et al.23   N2 3:322 log10 SGR N1 ¼ ð1Þ day T2  T1 where N1 and N2 are the number of cells at the initial (T1) and final (T2) times. Total Organic Carbon (TOC) Analysis. TOC analysis was performed on dried algae from the growth experiments according to the method entitled Determination of Organic Carbon and Nitrogen in Marine Sediments Using the Carlo Erba NA-1500 Analyzer.24 This value was used in the calculation of fixed CO2. Calculation of Fixed CO2. Assuming that all CO2 used by the algae is converted to biomass, the CO2 fixation rate of algae was calculated according to the equation FA ¼

μ  mcbm  MCO2 MC

ð2Þ

where FA is the rate of CO2 fixation per volume of algae (g of CO2 L1

day1), μ is the average growth rate over a study period (g of dry biomass L1 day1), mcbm is the mass fraction of organic carbon in the dry algal biomass (g of carbon/g of dry biomass), MCO2 is the molecular weight of CO2 (g of CO2/mol), and MC is the molecular weight of carbon (g of carbon/mol).21

’ RESULTS AND DISCUSSION Growth of C. pyrenoidosa in OSTW. An amendment of the MES-Volvox growth medium with up to 10% (v/v) tailings water had no effect on the growth rate of the algae. However, the addition of higher concentrations of tailings significantly stimulated growth (Figure 1). The algal growth rates for the 30 and 50% (v/v) tailings averaged over the entire study period were 0.088 and 0.085 g of dry biomass L1 day1, respectively. On the basis of this average growth rate, the CO2 fixation rates increased by a factor of 3, from approximately 0.033 g of CO2 L1 day1 for 0 and 10% tailings to 0.11 g of CO2 L1 day1 for 30 and 50% (v/v) tailings. Media Development and Optimization. The results of the full factorial experiment are given in Table 4. Minimal growth (1.2  106 cells/mL) was observed when none of the tested 1902

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Table 5. Experimental Results of the Central Composite Design for the Number of Cells, SGR, and Time Required To Attain the Maximum Cell Number number of days required

Figure 1. Growth of C. pyrenoidosa grown in static growth conditions with 0, 10, 30, and 50% (v/v) tailings added to MES-Volvox growth media.

Table 4. Experimental Results of the Full Factorial Run for the Number of Cells, SGR, and Time Required To Attain the Maximum Cell Number experiment number of cells number (1  106 cells/mL)

SGR

1

27.1 ( 1.3

0.26 ( 0.00

2

2.41 ( 0.05

0.29 ( 0.01

3

11.4 ( 0.20

0.31 ( 0.10

4

5.40 ( 0.17

0.74 ( 0.10

experiment

number of cells

number

(1  106 cells/mL)

to attain the maximum SGR

cell number (day) 9.5 ( 0.7

1

19.2 ( 4.0

0.41 ( 0.03

2

23.6 ( 2.1

0.52 ( 0.01

3 4

26.7 ( 2.7 20.5 ( 0.95

0.20 ( 0.01 0.23 ( 0.01

5

38.5 ( 2.1

0.39 ( 0.02

6

40.2 ( 2.6

0.21 ( 0.00

7

40.3 ( 2.3

0.28 ( 0.01

8

42.1 ( 1.9

0.31 ( 0.00

9 29 ( 1.4 26 13 27.5 ( 0.7 21 18.5 ( 0.1

9

24.5 ( 0.06

0.20 ( 0.01

29.5 ( 0.7

10

19.9 ( 3.8

0.20 ( 0.01

28.5 ( 0.7

11 12

20.1 ( 4.2 20.3 ( 1.9

0.19 ( 0.01 0.52 ( 0.01

30 9

13

41.2 ( 0.2

0.50 ( 0.04

9

14

43.1 ( 4.7

0.20 ( 0.01

28

15

43.9 ( 1.7

0.31 ( 0.01

16

46.4 ( 2.2

0.31 ( 0.01

18.5 ( 0.7

duration required to attain the

17

48.0 ( 0.6

0.31 ( 0.01

18.5 ( 0.7

maximum cell number (day)

18

43.4 ( 0.4

0.52 ( 0.04

9.5 ( 0.7

19 20

11.4 ( 0.2 42.3 ( 1.4

0.21 ( 0.01 0.31 ( 0.01

28.5 ( 0.7 19 8.5 ( 0.7

19 5

19

11.3 ( 0.6

21

42.4 ( 0

0.55 ( 0.03

3.33 ( 0.6

22

44.6 ( 0.25

0.19 ( 0.01

30

23

43.8 ( 0.20

0.24 ( 0.04

24

5

14.2 ( 1.1

0.27 ( 0.01

14

6

6.00 ( 0.32

0.90 ( 0.02

3

24

50.3 ( 0.25

0.31 ( 0.00

19

4 19

25

48.8 ( 0.63

0.20 ( 0.01

29 ( 1.4

26

52.4 ( 0

0.20 ( 0.01

28.5 ( 0.7

3

27 28

51.7 ( 1.1 53.4 ( 0.2

0.52 ( 0.06 0.35 ( 0.01

9.5 ( 0.7 17.5 ( 0.7

7 8

2.70 ( 0.29 38.6 ( 5.6

0.38 ( 0.04 0.28 ( 0.01

9

5.10 ( 0.30

0.81 ( 0.03

10

4.35 ( 0.03

0.72 ( 0.01

3

11

33.5 ( 0.40

0.27 ( 0.01

19

29

51.3 ( 3.1

0.32 ( 0.02

19 ( 1.4

5

30

50.8 ( 0.23

0.54 ( 0.00

8.5 ( 0.7

31

51.8 ( 1.8

0.31 ( 0.00

18.5 ( 0.7

12

3.48 ( 0.44

0.46 ( 0.04

13

11.5 ( 1.1

0.30 ( 0.02

14

53.2 ( 1.5

0.30 ( 0.02

15 16

1.27 ( 0.05 53.6 ( 1.0

0.12 ( 0.01 0.31 ( 0.01

10.7 ( 0.6 19 3 19.3 ( 0.6

media components was added to the defined algal medium (condition 15). Similarly, the addition of nitrates (condition 2), phosphate (condition 6), both nitrates and phosphates (condition 4), and the combination of all three components (condition 13) did not show growth of C. pyrenoidosa in OSTW. The addition of Fe-EDTA with phosphate and nitrates increased growth by more than an order of magnitude, to 54  106 cells/mL. The effect of the parameters can be described by an empirical model equation Ynumber of

cells

¼ 17:096 þ 3:045X1 þ 7:859X2

þ 13:28X3  1:425X4 þ 1:123X1 X2 þ 2:91X1 X3 þ 6:464X2 X3  0:489X1 X4 þ 0:605X2 X4 þ 1:449X3 X4 ð3Þ

where X1X4 are defined in Table 2. Fe-EDTA and phosphate exerted the strongest effect on growth (F e 0.0001), followed by sodium nitrate (F = 0.0001). The trace metal solution had a negative linear effect on the growth (F = 0.0412) (R2 = 0.97; F e 0.0001). The results of the second experimental design undertaken to determine the optimal concentrations of nitrate, phosphate, Fe-EDTA, and trace elements are given in Table 5. Growth of C. pyrenoidosa was adequately described (R2 = 0.94; F e 0.0001) by the second-order polynomial equation Ynumber of

cells

¼ 52:309 þ 0:0123X1 þ 9:681X2 þ 0:624X3

þ 0:586X4  3:193X1 2  9:212X2 2  3:903X3 2  2:771X4 2 þ 0:0203X1 X2  0:37X1 X3 þ 0:576X2 X3 ð4Þ where X1X4 are defined in Table 3. A visual representation of the effect of phosphate and nitrate can be seen in Figure 2. The optimum concentrations of sodium nitrate, phosphate, FeEDTA, and trace metal solution were found to be 11.9 mM, 9.41 mM, 49.5 μM, and 2 mL/L, respectively. 1903

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The conditions for the growth of the algae, of course, would be much different than the conditions found in the Athabasca oil sands. Some of these differences may include the following: (i) Tailings would most likely be unfiltered, and not clarified. (ii) Illumination would not occur at a constant rate at all times of each day if natural light was used as the light source. (iii) The amount of light reaching lower depths of tailings ponds would be less than the amount of light at the surface.25 (iv) Temperature would fluctuate during the day, throughout the seasons, and vary by location because of climate conditions and the temperature of the hot water extraction effluent. This scale-up result is therefore a very rough estimation but a valuable preliminary calculation. Further experimentation would be required to quantify the effects of variable illumination, tailings quality, and temperature.

Figure 2. Effect of phosphate and nitrate on the growth of C. pyrenoidosa.

Potential for CO2 Fixation by a Full-Scale System. To obtain an estimate of the potential for CO2 fixation in a fullscale system, calculations were based on the growth rate and CO2 fixation rate of 50% (v/v) tailings algal culture, which was 0.085 g of dry biomass L1 day1 and 0.11 g of CO2 L1 day1. For this calculation, the annual water use (349 million m3 of extracted water) was used as the reactor volume.22 The following empirical equations were used to obtain the scale-up results:

’ CONCLUSIONS C. pyrenoidosa can be grown in 95% OSTW as a mean of fixing CO2 and producing value-added products. Growth was optimized by amending the tailings water with phosphate (11.9 mM), sodium nitrate (9.41 mM), Fe-EDTA (49.5 μM), and trace metal solution (2.2 mL/L). On the basis of batch growth trials in the lab and not accounting for sub-optimal growth conditions in the full-scale system, approximately 12 million tons of CO2 could be fixed annually by growing this algae in the Athabasca tailings ponds. ’ AUTHOR INFORMATION Corresponding Author

VT ¼ 0:9  VW  1000

ð5Þ

*Telephone: 604-822-9485. sduff@chbe.ubc.ca.

VT  μ50  365 106

ð6Þ

VT  FA 50  365 106

ð7Þ

’ ACKNOWLEDGMENT The following individuals are gratefully acknowledged for their support throughout this study: Donna Dinh of the Canadian Centre for the Culture of Microorganisms for her advice on culturing algae and providing the stock culture of C. pyrenoidosa, Maureen Soon of UBC Oceanography for performing the TOC analysis, and Justin Matsui and Michael Lee for their laboratory guidance.

mbio ¼ mCO2 ¼

CC ¼ mCO2 PC

ð8Þ

where VT is the volume of tailings produced per year (L), VW is the volume of process water used per year in oil sands (m3), mbio is the annual amount of dry biomass produced by algae (tonnes), μ50 is the average growth rate of the 50% (v/v) tailings algal culture (g of dry biomass L1 day1), mCO2 is the annual amount of CO2 fixed by algae grown in tailings ponds (tonnes), FA50 is the CO2 fixation rate of the 50% (v/v) tailings algal culture (g of CO2 L1 day1), CC is the annual value of carbon credits associated with the amount of CO2 fixed ($ CDN), and PC is the selling price per ton of CO2 for carbon credits assumed to be between $5 and 25 CDN/ton. On the basis of these calculations, algae grown in Athabasca oil sands tailings ponds could potentially fix 12 million tonnes of CO2 per year; a carbon credit value of $60 to 300 million CDN. The actual growth rate and CO2 fixation rate in a full-scale system would likely be reduced by suboptimal growing conditions; however, even a fraction of this value would be a significant proportion of oil sands emissions. The amount of dry algal biomass produced would be 10 million tons per year, biomass that could be used to produce biofuels, such as methane or biodiesel.

Fax:

604-822-6003.

E-mail:

’ REFERENCES (1) Wu, M.; Mintz, M.; Wang, M.; Arora, S. Environ. Manage. 2009, 44, 981–997. (2) Gentes, M.; Waldner, C.; Papp, Z.; Smits, J. E. G. J. Toxicol. Environ. Health 2007, 70, 1182–1190. (3) Quagraine, E. K.; Peterson, H. G.; Headley, J. V. J. Toxicol. Environ. Health 2005, 40, 685–722. (4) Clemente, J. S.; Fedorak, P. M. Chemosphere 2005, 60, 585–600. (5) Han, X. M.; MacKinnon, M. D.; Martin, J. W. Chemosphere 2009, 76, 63–70. (6) Herman, D. C.; Fedorak, P. M.; Costerton, J. W. Can. J. Microbiol. 1993, 39, 576–580. (7) Herman, D. C.; Fedorak, P. M.; Mackinnon, M. D.; Costerton, J. W. Can. J. Microbiol. 1994, 40, 467–477. (8) Renault, S.; Lait, C.; Zwiazek, J. J.; MacKinnon, M. Environ. Pollut. 1998, 102, 177–184. (9) Warith, M. A.; Yong, R. N. Environ. Technol. 1994, 15, 381–387. (10) Whitby, C. Microbial naphthenic acid degradation. In Advances in Applied Microbiology; Laskin, A. I., Sariaslani, S., Gadd, G. M., Eds.; Academic Press: New York, 2010; pp 93125. 1904

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dx.doi.org/10.1021/ef101503h |Energy Fuels 2011, 25, 1900–1905