Please wait a minute...
Shopping Cart Email List Chinese
Advanced Search Fig/Tab
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Featured Articles  |  Most Downloaded  |  Most Reading
Online Submission Subscribe to Our RSS Content Feed
Front Envir Sci Eng    2014, Vol. 8 Issue (2) : 293-304    https://doi.org/10.1007/s11783-013-0561-9
RESEARCH ARTICLE
Bioremediation of highly contaminated oilfield soil: Bioaugmentation for enhancing aromatic compounds removal
Jun QIAO1,2, Chengdong ZHANG1,3,4(), Shuiming LUO1, Wei CHEN1,3,4()
1. College of Environmental Science and Engineering, Nankai University, Tianjin 300071, China; 2. College of Chemistry and Environmental Engineering, Shanxi Datong University, Datong 037009, China; 3. Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Tianjin 300071, China; 4. Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Tianjin 300071, China
 Download: PDF(414 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

This study evaluated the effectiveness of different amendments—including a commercial NPK fertilizer, a humic substance (HS), an organic industrial waste (NovoGro), and a yeast-bacteria consortium—in the remediation of highly contaminated (up to 6% of total petroleum hydrocarbons) oilfield soils. The concentrations of hydrocarbon, soil toxicity, physicochemical properties of the soil, microbial population numbers, enzyme activities and microbial community structures were examined during the 90-d incubation. The results showed that the greatest degradation of total petroleum hydrocarbons (TPH) was observed with the biostimulation using mixture of NPK, HS and NovoGro, a treatment scheme that enhanced both dehydrogenase and lipase activities in soil. Introduction of exogenous hydrocarbon-degrading bacteria (in addition to biostimulation with NPK, HS and NovoGro) had negligible effect on the removal of TPH, which was likely due to the competition between exogenous and autochthonous microorganisms. Nonetheless, the addition of exogenous yeast-bacteria consortium significantly enhanced the removal of the aromatic fraction of the petroleum hydrocarbons, thus detoxifying the soil. The effect of bioaugmentation on the removal of more recalcitrant petroleum hydrocarbon fraction was likely due to the synergistic effect of bacteria and fungi.
Keywords bioremediation      petroleum hydrocarbon      biostimulation      bioaugmentation     
Corresponding Author(s): ZHANG Chengdong,Email:zhangchengdong@nankai.edu.cn; CHEN Wei,Email:chenwei@nankai.edu.cn   
Issue Date: 01 April 2014
 Cite this article:   
Jun QIAO,Chengdong ZHANG,Shuiming LUO, et al. Bioremediation of highly contaminated oilfield soil: Bioaugmentation for enhancing aromatic compounds removal[J]. Front Envir Sci Eng, 2014, 8(2): 293-304.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-013-0561-9
https://academic.hep.com.cn/fese/EN/Y2014/V8/I2/293
itemtreatmentstotalpetroleum hydrocarbonpetroleum hydrocarbon fraction a)
saturatesaromatics
percentage of degradation / %NA11.45±0.43 c c)15.47±2.35 c9.30±2.97 c
F37.55±1.48 b56.60±1.21 b20.26±0.94 b
FH37.75±1.88 b55.97±1.07 b18.84±2.32 b
FHN41.90±0.98 a61.92±0.31 a24.72±3.01 b
FNMM37.10±0.61 b60.20±2.36 ab32.43±1.04 a
first-order rate constant k /(d-1) b), half-life t1/2 /(days) and (r2)F0.0298, 23.26 (0.9463)0.0266, 26.06 (0.9696)0.0081, 85.57 (0.7218)
FH0.0364, 19.04 (0.9783)0.0371, 18.68 (0.9354)0.0060, 115.52 (0.9228)
FHN0.0617, 11.23 (0.9339)0.0584, 11.87 (0.9016)0.0076, 91.20 (0.9346)
FHNM0.0504, 13.75 (0.8992)0.0361, 19.20 (0.9492)0.0251, 27.62 (0.9083)
Tab.1  Cumulative percentage of degradation after 90 d and rate constant of degradation of total petroleum hydrocarbon and different fractions
Fig.1  Biodegradation of 16 PAHs (a) and toxicity assays (b) after 90 d in different treatment schemes. The same letter indicated not statistical difference among treatments at the same sampling time by the Tukey test (<0.05). Error bards represent standard deviations ( = 3). The 16 PAHs were classified in the groups according to the number of aromatic rings. 2-rings PAHs contain naphthalene, acenaphthylene, acenaphthene and fluorene. 3-4 rings PAHs contain phenanthrene, anthracene, fluoranthene, pyrene, benzo()anthracene, chrysene, benzo()fluoranthene and benzo()fluoranthene. 5-6 rings PAHs contain Benzo()pyrene, Indeno(1,2,3-)pyrene, dibenzo(,)anthracene and benzo(,,)perylene
soil nutrientstreatmentstime /d
01545
carbon /(g·kg-1)NA71.98±0.57 a a)69.17±2.17 a70.77±1.39 a
F64.30±0.29 a64.79±0.57 a55.47±0.03 b
FH67.87±1.64 a71.20±1.76 a64.91±1.80 a
FHN71.40±0.74 a67.98±0.90 b60.96±0.41 c
FHNM77.61±0.57 a76.89±0.78 a68.73±0.33 b
nitrogen /(mg·kg-1)NA57.38±1.07 a32.42±1.57 c46.36±1.61 b
F605.96±2.42 a182.79±1.01 b175.95±1.07 c
FH743.41±34.84 a238.36±2.68 b198.57±10.42 b
FHN646.81±9.67 a259.56±4.84 c314.28±0.54 b
FHNM761.20±15.05 a304.41±20.43 b258.50±1.61 b
phosphorous/(mg·kg-1)NA6.43±0.28 a4.49±0.28 b2.39±0.00 c
F98.19±0.00 a79.81±2.26 b40.24±3.01 c
FH101.62±13.70 a59.61±6.51 b50.51±0.49 b
FHN187.18±7.96 a132.05±0.00 b127.22±1.37 b
FHNM84.59±0.54 a72.51±4.91 ab64.98±0.82 b
Tab.2  Effects of different treatments on available soil nutrients during incubation
Fig.2  Changes in counts of total heterotrophic bacteria (a), and hydrocarbon degrading microorganisms (b) in different treatments. The same letter indicated not statistical difference among treatments at the same sampling time by the Tukey test (<0.05). Error bars represent standard deviations ( = 3)
microbial activitytreatmentstime /d
071530456090
dehydrogenase activities / (μg TPF·g-1 soil)NA18.78±3.01 c a565.62±19.78 c689.75±35.08 c698.89±29.62 c700.92±16.06 e739.84±12.85 b900.15±23.41 c
F89.94±10.38 b2366.71±170.05 b2739.38±173.06 ab3176.06±130.55 a2481.27±85.18 b2077.58±57.13 a1497.78±157.40 a
FH118.85±1.55 b2247.16±180.36 b2600.38±239.69 b2343.25±184.03 b1864.74±93.67 c502.32±39.66 c1241.99±128.64 b
FHN158.87±30.32 a3314.33±230.43 a3229.83±83.43 a3195.36±103.11 a2956.81±67.87 a310.20±72.16 d708.77±129.76 cd
FHNM90.34±13.31 b3105.25±154.77 a2261.82±186.59 b1971.89±29.62 b1316.83±69.91 d421.85±12.04 cd551.18±74.48 d
FDA hydrolase activities / (μg fluorescein·g-1 soil)NA13.00±0.31 c84.85±8.96 c123.50±3.51 c136.38±2.40 d127.78±1.31 c149.90±5.39 b153.32±2.15 a
F16.11±1.77 bc157.71±1.07 b159.83±6.60 ab162.64±4.89 bc166.97±5.20 ab172.01±2.49 a155.48±11.18 a
FH18.23±0.14 ab147.41±4.47 b158.49±4.53 ab149.16±5.30 cd156.11±3.35 b172.62±4.77 a164.82±6.81 a
FHN21.40±0.65 a177.40±7.88 a171.60±5.57 a166.49±2.46 b170.21±1.50 a155.37±10.22 b170.56±0.32 a
FHNM16.48±4.28 bc180.55±2.98 a152.00±4.99 b188.79±6.88 a176.37±5.35 a176.35±3.53 a158.90±1.49 a
lipase activities /(·g pNP·g-1 soil)NA213.96±11.37 b719.14±142.11 c1127.06±27.74 c1020.01±201.45 d1548.81±39.39 d1001.83±17.79 c400.81±94.05 c
F227.94±45.46 b3021.61±136.86 b1154.56±59.41 c5146.89±173.11 b1262.39±10.42 d2265.90±123.61 b1542.58±216.44 b
FH176.29±4.33 b3357.50±304.96 b1290.45±22.84 c5701.81±146.37 b5233.20±276.63 b2393.07±41.73 b1700.67±313.57 b
FHN339.95±57.24 a6451.39±310.04 a5480.04±241.75 a8907.85±638.51 a5822.23±246.27 a6092.89±565.17 a4520.95±421.44 a
FHNM195.47±20.47 b1090.60±225.73 c4158.50±82.89 b3231.28±309.38 c4466.99±88.52 c1227.37±56.81 c1229.65±53.65 b
Tab.3  Changes in microbial activity with different treatments during bioremediation
treatmentsparameter b)correlation coefficients
DHNFDALIPTHBHDMSATARO
FHTPH0.659**-0.560*-0.1610.2520.4030.980**0.432
DHN-0.723**0.1900.714**0.576*0.598*0.764**
FDA-0.491-0.624*-0.555*-0.592**-0.428
LIP0.713**0.651*-0.0670.143
THB0.750**0.2700.714**
HDM0.4300.538
SAT0.367
FHNTPH0.760**0.535*0.3800.680**0.721**0.969**0.820**
DHN0.5560.5120.790**0.814**0.750**0.625*
FDA-0.0910.1840.2150.542*0.379
LIP0.892**0.724**0.4480.726**
THB0.913**0.681**0.826**
HDM0.784**0.772**
SAT0.773**
FHNMTPH0.827**0.037-0.2110.2290.2080.969**0.769**
DHN0.0220.1660.4510.540*0.896*0.790**
FDA-0.186-0.501-0.133-0.0510.531
LIP0.704**0.727**-0.002-0.409
THB0.761**0.428-0.123
HDM0.3780.111
SAT0.704**
Tab.4  Correlation matrix of hydrocarbon decontamination and soil biologic parameters
Fig.3  DGGE fingerprints of 16S rDNA fragments in soil samples from FHN and FHNM treatments (a), and the diagram sketch (b) obtained by Quantity One image analysis software. The numbers above the lanes refer to samples from different treatments at different times: (1) FHNM, 60 d; (2) FHNM, 30 d; (3) FHNM, 15 d; (4) FHNM, 7 d; (5) FHNM, 0 d; (6) FHN, 60 d; (7) FHN, 30 d; (8) FHN, 15 d; (9) FHN, 7 d; (10) FHN, 0 d
indextreatmentstime /d
07153060
Shannon–Wiener diversity indexFHN1.542.232.362.542.48
FHNM2.332.342.282.272.13
Evenness indexFHN0.740.820.900.900.88
FHNM0.820.830.820.860.81
Abundance (the total number of bands)FHN815141717
FHNM1717161414
Tab.5  Changes of bacterial genetic diversities based on DGGE profiles under FHN and FHNM treatments
1 Sarkar D, Ferguson M, Datta R, Birnbaum S. Bioremediation of petroleum hydrocarbons in contaminated soils: comparison of biosolids addition, carbon supplementation, and monitored natural attenuation. Environmental pollution , 2005, 136(1): 187-195
doi: 10.1016/j.envpol.2004.09.025 pmid:15809120
2 Adesodun J K, Mbagwu J S C. Biodegradation of waste-lubricating petroleum oil in a tropical alfisol as mediated by animal droppings. Bioresource Technology , 2008, 99(13): 5659-5665
doi: 10.1016/j.biortech.2007.10.031 pmid:18036815
3 Fava F, Berselli S, Conte P, Piccolo A, Marchetti L. Effects of humic substances and soya lecithin on the aerobic bioremediation of a soil historically contaminated by polycyclic aromatic hydrocarbons (PAHs). Biotechnology and Bioengineering , 2004, 88(2): 214-223
doi: 10.1002/bit.20225 pmid:15449300
4 Lee S H, Oh B I, Kim J G. Effect of various amendments on heavy mineral oil bioremediation and soil microbial activity. Bioresource Technology , 2008, 99(7): 2578-2587
doi: 10.1016/j.biortech.2007.04.039 pmid:17572087
5 Margesin R, Schinner F. Efficiency of indigenous and inoculated cold-adapted soil microorganisms for biodegradation of diesel oil in alpine soils. Applied and Environmental Microbiology , 1997, 63(7): 2660-2664
pmid:16535642
6 Bento F M, Camargo F A O, Okeke B C, Frankenberger W T. Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresource Technology , 2005, 96(9): 1049-1055
doi: 10.1016/j.biortech.2004.09.008 pmid:15668201
7 Karamalidis A K, Evangelou A C, Karabika E, Koukkou A I, Drainas C, Voudrias E A. Laboratory scale bioremediation of petroleum-contaminated soil by indigenous microorganisms and added Pseudomonas aeruginosa strain Spet. Bioresource Technology , 2010, 101(16): 6545-6552
doi: 10.1016/j.biortech.2010.03.055 pmid:20400304
8 van Herwijnen R, Joffe B, Ryngaert A, Hausner M, Springael D, Govers H A J, Wuertz S, Parsons J R. Effect of bioaugmentation and supplementary carbon sources on degradation of polycyclic aromatic hydrocarbons by a soil-derived culture. FEMS Microbiology Ecology , 2006, 55(1): 122-135
doi: 10.1111/j.1574-6941.2005.00001.x pmid:16420621
9 Liu W X, Luo Y M, Teng Y, Li Z G, Christie P. Prepared bed bioremediation of oily sludge in an oilfield in northern China. Journal of Hazardous Materials , 2009, 161(1): 479-484
doi: 10.1016/j.jhazmat.2008.03.123 pmid:18572312
10 Antizar-Ladislao B, Lopez-Real J, Beck A J. Laboratory studies of the remediation of polycyclic aromatic hydrocarbon contaminated soil by in-vessel composting. Waste Management (New York, N.Y.) , 2005, 25(3): 281-289
doi: 10.1016/j.wasman.2005.01.009 pmid:15823743
11 P?aza G, Na?ecz-Jawecki G, Ulfig K, Brigmon R L. The application of bioassays as indicators of petroleum-contaminated soil remediation. Chemosphere , 2005, 59(2): 289-296
doi: 10.1016/j.chemosphere.2004.11.049 pmid:15722101
12 Trindade P V O, Sobral L G, Rizzo A C L, Leite S G F, Soriano A U. Bioremediation of a weathered and a recently oil-contaminated soils from Brazil: a comparison study. Chemosphere , 2005, 58(4): 515-522
doi: 10.1016/j.chemosphere.2004.09.021 pmid:15620743
13 Wrenn B A, Venosa A D. Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Canadian Journal of Microbiology , 1996, 42(3): 252-258
doi: 10.1139/m96-037 pmid:8868232
14 Margesin R, Walder G, Schinner F. The impact of hydrocarbon remediation (diesel oil and polycyclic aromatic hydrocarbons) on enzyme activities and microbial properties of soil. Acta Biotechnologica , 2000, 20(3-4): 313-333
doi: 10.1002/abio.370200312
15 Bao S D. Analytical Methods of Soil Agricultural Chemistry. 3rd ed. Beijing: China Agricultural Science Press, 2005 (in Chinese)
16 Haderlein A, Legros R, Ramsay B. Enhancing pyrene mineralization in contaminated soil by the addition of humic acids or composted contaminated soil. Applied Microbiology and Biotechnology , 2001, 56(3-4): 555-559
doi: 10.1007/s002530000520 pmid:11549037
17 Tejada M, Gonzalez J L, Hernandez M T, Garcia C. Application of different organic amendments in a gasoline contaminated soil: effect on soil microbial properties. Bioresource Technology , 2008, 99(8): 2872-2880
doi: 10.1016/j.biortech.2007.06.002 pmid:17662598
18 Samanta S K, Singh O V, Jain R K. Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends in Biotechnology , 2002, 20(6): 243-248
doi: 10.1016/S0167-7799(02)01943-1 pmid:12007492
19 Barathi S, Vasudevan N. Utilization of petroleum hydrocarbons by Pseudomonas fluorescens isolated from a petroleum-contaminated soil. Environment International , 2001, 26(5-6): 413-416
doi: 10.1016/S0160-4120(01)00021-6 pmid:11392760
20 Calvo C, Toledo F L, González-López J. Surfactant activity of a naphthalene degrading Bacillus pumilus strain isolated from oil sludge. Journal of Biotechnology , 2004, 109(3): 255-262
doi: 10.1016/j.jbiotec.2004.01.009 pmid:15066763
21 Qi J C, Zhang C D, Qiao J, Guo T, Zhang Q M, Chen W. Bioremediation of petroleum contaminated soil by mixed microbes and organic fertilizer. Journal of Agro-Environment Science , 2010, 29(1): 66-72 (in Chinese)
22 MacGillivray A R, Shiaris M P. Biotransformation of polycyclic aromatic hydrocarbons by yeasts isolated from coastal sediments. Applied and Environmental Microbiology , 1993, 59(5): 1613-1618
pmid:8517753
23 Han H L, Tang J, Jiang H, Zhang M L, Liu Z. Synergy between fungi and bacteria in fungi-bacteria augmented remediation of petroleum-contaminated soil. Environmental Science , 2008, 29(1): 189-195 (in Chinese)
pmid:18441939
24 Margesin R, Schinner F. Bioremediation (natural attenuation and biostimulation) of diesel-oil-contaminated soil in an alpine glacier skiing area. Applied and Environmental Microbiology , 2001, 67(7): 3127-3133
doi: 10.1128/AEM.67.7.3127-3133.2001 pmid:11425732
25 Laconi S, Molle G, Cabiddu A, Pompei R. Bioremediation of olive oil mill wastewater and production of microbial biomass. Biodegradation , 2007, 18(5): 559-566
doi: 10.1007/s10532-006-9087-1 pmid:17103247
26 Dubey K, Juwarkar A. Distillery and curd whey wastes as viable alternative sources for biosurfactant production. World Journal of Microbiology and Biotechnology , 2001, 17(1): 61-69
doi: 10.1023/A:1016606509385
27 Embar K, Forgacs C, Sivan A. The role of indigenous bacterial and fungal soil populations in the biodegradation of crude oil in a desert soil. Biodegradation , 2006, 17(4): 369-377
doi: 10.1007/s10532-005-9007-9 pmid:16570229
28 Jacques R J S, Okeke B C, Bento F M, Teixeira A S, Peralba M C R, Camargo F A O. Microbial consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated soil. Bioresource Technology , 2008, 99(7): 2637-2643
doi: 10.1016/j.biortech.2007.04.047 pmid:17572084
29 Kim J D, Lee C G. Microbial degradation of polycyclic aromatic hydrocarbons in soil by bacterium-fungus co-cultures. Biotechnology and Bioprocess Engineering , 2007, 12(4): 410-416
doi: 10.1007/BF02931064
30 Wick L Y, Remer R, Würz B, Reichenbach J, Braun S, Sch?fer F, Harms H. Effect of fungal hyphae on the access of bacteria to phenanthrene in soil. Environmental Science and Technology , 2007, 41(2): 500-505
doi: 10.1021/es061407s pmid:17310713
[1] Karla Ilić Đurđić, Raluca Ostafe, Olivera Prodanović, Aleksandra Đurđević Đelmaš, Nikolina Popović, Rainer Fischer, Stefan Schillberg, Radivoje Prodanović. Improved degradation of azo dyes by lignin peroxidase following mutagenesis at two sites near the catalytic pocket and the application of peroxidase-coated yeast cell walls[J]. Front. Environ. Sci. Eng., 2021, 15(2): 19-.
[2] Ling Huang, Syed Bilal Shah, Haiyang Hu, Ping Xu, Hongzhi Tang. Pollution and biodegradation of hexabromocyclododecanes: A review[J]. Front. Environ. Sci. Eng., 2020, 14(1): 11-.
[3] Yueqiao Liu, Aizhong Ding, Yujiao Sun, Xuefeng Xia, Dayi Zhang. Impacts of n-alkane concentration on soil bacterial community structure and alkane monooxygenase genes abundance during bioremediation processes[J]. Front. Environ. Sci. Eng., 2018, 12(5): 3-.
[4] Lifeng Cao, Weihua Sun, Yuting Zhang, Shimin Feng, Jinyun Dong, Yongming Zhang, Bruce E. Rittmann. Competition for electrons between reductive dechlorination and denitrification[J]. Front. Environ. Sci. Eng., 2017, 11(6): 14-.
[5] Qingliang Zhao, Hang Yu, Weixian Zhang, Felix Tetteh Kabutey, Junqiu Jiang, Yunshu Zhang, Kun Wang, Jing Ding. Microbial fuel cell with high content solid wastes as substrates: a review[J]. Front. Environ. Sci. Eng., 2017, 11(2): 13-.
[6] Ying Xu, Ning-Yi Zhou. Microbial remediation of aromatics-contaminated soil[J]. Front. Environ. Sci. Eng., 2017, 11(2): 1-.
[7] Chong Liu, Jianzheng Li, Shuo Wang, Loring Nies. A syntrophic propionate-oxidizing microflora and its bioaugmentation on anaerobic wastewater treatment for enhancing methane production and COD removal[J]. Front. Environ. Sci. Eng., 2016, 10(4): 13-.
[8] Wendi XU,Shuhai GUO,Gang LI,Fengmei LI,Bo WU,Xinhong GAN. Combination of the direct electro-Fenton process and bioremediation for the treatment of pyrene-contaminated soil in a slurry reactor[J]. Front. Environ. Sci. Eng., 2015, 9(6): 1096-1107.
[9] Mary Beth LEIGH,Wei-Min WU,Erick CARDENAS,Ondrej UHLIK,Sue CARROLL,Terry GENTRY,Terence L. MARSH,Jizhong ZHOU,Philip JARDINE,Craig S. CRIDDLE,James M. TIEDJE. Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing[J]. Front. Environ. Sci. Eng., 2015, 9(3): 453-464.
[10] Di CUI,Ang LI,Tian QIU,Rui CAI,Changlong PANG,Jihua WANG,Jixian YANG,Fang MA,Nanqi REN. Improvement of nitrification efficiency by bioaugmentation in sequencing batch reactors at low temperature[J]. Front. Environ. Sci. Eng., 2014, 8(6): 937-944.
[11] Shuang LIU, Yanwei HOU, Guoxin SUN. Synergistic degradation of pyrene and volatilization of arsenic by cocultures of bacteria and a fungus[J]. Front Envir Sci Eng, 2013, 7(2): 191-199.
[12] Dengqiang FU, Ying TENG, Yuanyuan SHEN, Mingming SUN, Chen TU, Yongming LUO, Zhengao LI, Peter CHRISTIE. Dissipation of polycyclic aromatic hydrocarbons and microbial activity in a field soil planted with perennial ryegrass[J]. Front Envir Sci Eng, 2012, 6(3): 330-335.
[13] Jiying NING, Gang GANG, Zhihui BAI, Qing HU, Hongyan QI, Anzhou MA, Xuliang ZHUAN, Guoqiang ZHUANG. In situ enhanced bioremediation of dichlorvos by a phyllosphere Flavobacterium strain[J]. Front Envir Sci Eng, 2012, 6(2): 231-237.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed