Bioprocess and Biosystems Engineering

, Volume 42, Issue 4, pp 643–655 | Cite as

Regulation of different electron acceptors on petroleum hydrocarbon biotransformation to final products in activated sludge biosystems

  • Lanmei Zhao
  • Congcong Zhang
  • Haoshuai Li
  • Mutai BaoEmail author
  • Peiyan Sun
Research Paper


The types and concentrations of electron acceptor are the significant factors influencing the oxidation and biotransformation of organic matter in the process of pollutant biodegradation. Regulation of O2, SO42− and NO3 as electron acceptors on petroleum hydrocarbon biotransformation to final products was studied using the multiple methods including mesoscale biodegradation experiments, thermodynamic theoretical calculations and stoichiometric analyses. Petroleum hydrocarbon biodegradation ratio (PHBR) rose from 64.7 to 82.4% with dissolved oxygen (DO) (3–5 mg L− 1). PHBR increased from 57.4 to 66.1% in SO42−-reducing biosystems and rose from 65.0 to 77.9% in NO3-reducing biosystems. Carbon balance was verified in different cultures. The shared functional microorganisms in different biosystems included Candida, Rhodococcus, Pseudomonas, Ochrobactrum, Marinobacter, Bacillus, Azoarcus, Alcanivorax, Acinetobacter. Pandoraea, Enterobacter and Burkholderia in anaerobic biosystems preferred to use NO3 and SO42− as electron acceptors for metabolism, and order of availability followed: NO3 > SO42−. Thermodynamic constraint showed that potentials of alkanes biotransformation to methane through hydrogenotrophic and acetoclastic methanogenesis in NO3-reducing biosystems were 7.27–7.73 and 7.25–7.70 times larger than those of SO42−-reducing biosystems, respectively. Metabolism equations of microorganisms proved that anabolism and catabolism on alkanes were feasible. This work provides a support for studying the biochemical process of petroleum hydrocarbon biotransformation and lays a foundation for the realization of oil-containing wastewater bioremediation.


Petroleum hydrocarbon Biotransformation Electron acceptor Functional microorganism Thermodynamic constraint 



This study was financially supported by the Fundamental Research Funds for the Central Universities (201861016), the National Key Research and Development Program (2016YFC1402301), the National Natural Science Foundation of China (41376084; 51174181), the Open Foundation of Key Laboratory of Marine Spill Oil Identification and Damage Assessment Technology of SOA (201702), the Key Research and Development Program of Shandong Province (public welfare special project) (2017GSF217012) and the Major Projects of the National High Technology Research and Development Program 863 (2013AA064401).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

449_2019_2070_MOESM1_ESM.doc (248 kb)
Supplementary material 1 (DOC 247 KB)


  1. 1.
    Zhang CC, Zhao LM, Bao MT, Lu JR (2018) Potential of hydrolyzed polyacrylamide biodegradation to final products through regulating its own nitrogen transformation in different dissolved oxygen systems. Bioresour Technol 256:61–68CrossRefGoogle Scholar
  2. 2.
    Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286CrossRefGoogle Scholar
  3. 3.
    Abid A, Saidane F, Hamdi M (2017) Feasibility of carbon dioxide sequestration by Spongiochloris sp microalgae during petroleum wastewater treatment in airlift bioreactor. Bioresour Technol 234:297–302CrossRefGoogle Scholar
  4. 4.
    Chen CM, Liang JH, Yoza BA, Li QX, Zhan YL, Wang QH (2017) Evaluation of an up-flow anaerobic sludge bed (UASB) reactor containing diatomite and maifanite for the improved treatment of petroleum wastewater. Bioresour Technol 243:620–627CrossRefGoogle Scholar
  5. 5.
    Demeter MA, Lemire JA, Mercer SM, Turner RJ (2017) Screening selectively harnessed environmental microbial communities for biodegradation of polycyclic aromatic hydrocarbons in moving bed biofilm reactors. Bioresour Technol 228:116–124CrossRefGoogle Scholar
  6. 6.
    Li JH, Sun SS, Yan P, Fang L, Yu Y, Xiang YD, Wang D, Gong YJ, Gong YJ, Zhang ZZ (2017) Microbial communities in the functional areas of a biofilm reactor with anaerobic–aerobic process for oily wastewater treatment. Bioresour Technol 238:7–15CrossRefGoogle Scholar
  7. 7.
    Cai MM, Yao J, Yang HJ, Wang RX, Masakorala K (2013) Aerobic biodegradation process of petroleum and pathway of main compounds in water flooding well of Dagang oil field. Bioresour Technol 144:100–106CrossRefGoogle Scholar
  8. 8.
    Dolfing J, Larter SR, Head IM (2008) Thermodynamic constraints on methanogenic crude oil biodegradation. ISME J 2(4):442–452CrossRefGoogle Scholar
  9. 9.
    Zhao LM, Zhang CC, Bao MT, Lu JR (2018) Effects of different electron acceptors on the methanogenesis of hydrolyzed polyacrylamide biodegradation in anaerobic activated sludge systems. Bioresour Technol 247:759–768CrossRefGoogle Scholar
  10. 10.
    Qiao W, Takayanagi K, Li Q, Shofie M, Gao F, Dong R, Li YY (2016) Thermodynamically enhancing propionic acid degradation by using sulfate as an external electron acceptor in a thermophilic anaerobic membrane reactor. Water Res 106:320–329CrossRefGoogle Scholar
  11. 11.
    Sabumon PC (2009) Effect of potential electron acceptors on anoxic ammonia oxidation in the presence of organic carbon. J Hazard Mater 172(1):280–288CrossRefGoogle Scholar
  12. 12.
    Shen J, Chen Y, Wu S, Wu H, Liu X, Sun X, Li J, Wang L (2015) Enhanced pyridine biodegradation under anoxic condition: the key role of nitrate as the electron acceptor. Chem Eng J 277:140–149CrossRefGoogle Scholar
  13. 13.
    An D, Caffrey SM, Soh J et al (2013) Metagenomics of hydrocarbon resource environments indicates aerobic taxa and genes to be unexpectedly common. Environ Sci Technol 47(18):10708–10717CrossRefGoogle Scholar
  14. 14.
    Varjani SJ, Gnansounou E (2017) Microbial dynamics in petroleum oilfields and their relationship with physiological properties of petroleum oil reservoirs. Bioresour Technol 245:1258–1265CrossRefGoogle Scholar
  15. 15.
    Wang D, Wang Y, Liu Y, Ngo HH, Lian Y, Zhao J, Chen F, Yang Q, Zeng G, Li X (2017) Is denitrifying anaerobic methane oxidation-centered technologies a solution for the sustainable operation of wastewater treatment plants? Bioresour Technol 234:456–465CrossRefGoogle Scholar
  16. 16.
    Colón J, Cadena E, Pognani M, Barrena R, Sánchez A, Font X, Artola A (2012) Determination of the energy and environmental burdens associated with the biological treatment of source-separated municipal solid wastes. Energy Environ Sci 5(2):5731–5741CrossRefGoogle Scholar
  17. 17.
    Pi YR, Bao MT, Liu YQ, Lu TY, He R (2017) The contribution of chemical dispersants and biosurfactants on crude oil biodegradation by Pseudomonas sp. LSH-7′. J Clean Prod 153:74–82CrossRefGoogle Scholar
  18. 18.
    Li XY, Yang SF (2007) Influence of loosely bound extracellular polymeric substances (EPS) on the flocculation, sedimentation and dewaterability of activated sludge. Water Res 41:1022–1030CrossRefGoogle Scholar
  19. 19.
    Sarkar P, Roy A, Pal S, Mohapatra B, Kazy SK, Maiti MK, Sar P (2017) Enrichment and characterization of hydrocarbon-degrading bacteria from petroleum refinery waste as potent bioaugmentation agent for in situ bioremediation. Bioresour Technol 242:15–27CrossRefGoogle Scholar
  20. 20.
    Xu NN, Bao MT, Sun PY, Li YM (2013) Study on bioadsorption and biodegradation of petroleum hydrocarbons by a microbial consortium. Bioresour Technol 149:22–30CrossRefGoogle Scholar
  21. 21.
    Guo CM, Chen Y, Chen JF, Wang XJ, Zhang GQ, Wang JX, Cui WF, Zhang ZZ (2014) Combined hydrolysis acidification and bio-contact oxidation system with air-lift tubes and activated carbon bioreactor for oilfield wastewater treatment. Bioresour Technol 169:630–636CrossRefGoogle Scholar
  22. 22.
    Tao KY, Liu XY, Chen XP, Hu XX, Cao LY, Yuan XY (2017) Biodegradation of crude oil by a defined co-culture of indigenous bacterial consortium and exogenous Bacillus subtilis. Bioresour Technol 224:327–332CrossRefGoogle Scholar
  23. 23.
    Varjani SJ, Upasani VN (2016) Biodegradation of petroleum hydrocarbons by oleophilic strain of Pseudomonas aeruginosa NCIM 5514. Bioresour Technol 222:195–201CrossRefGoogle Scholar
  24. 24.
    Roy A, Dutta A, Pal S, Gupta A, Sarkar J, Chatterjee A, Anumeha S, Poulomi S, Pinaki S, Kazy SK (2018) Biostimulation and bioaugmentation of native microbial community accelerated bioremediation of oil refinery sludge. Bioresour Technol 253:22–32CrossRefGoogle Scholar
  25. 25.
    Pi YR, Chen B, Bao MT, Fan FQ, Cai QH, Ze L, Zhang BY (2017) Microbial degradation of four crude oil by biosurfactant producing strain Rhodococcus sp. Bioresour Technol 232:263–269CrossRefGoogle Scholar
  26. 26.
    Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37:5701–5710CrossRefGoogle Scholar
  27. 27.
    Yamashita Y, Tanoue E (2003) Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids. Mar Chem 82:255–271CrossRefGoogle Scholar
  28. 28.
    Wang ZP, Zhang T (2010) Characterization of soluble microbial products (SMP) under stressful conditions. Water Res 44:5499–5509CrossRefGoogle Scholar
  29. 29.
    Barreto RVG, Hissa DC, Paes FA, Grangeiro TB, Nascimento RF, Rebelo LM, Craveiro AA, Melo VMM (2010) New approach for petroleum hydrocarbon degradation using bacterial spores entrapped in chitosan beads. Bioresour Technol 101(7):2121–2125CrossRefGoogle Scholar
  30. 30.
    Zhang ZZ, Hou ZW, Yang CY, Ma CQ, Tao F, Xu P (2011) Degradation of n-alkanes and polycyclic aromatic hydrocarbons in petroleum by a newly isolated Pseudomonas aeruginosa DQ8. Bioresour Technol 102(5):4111–4116CrossRefGoogle Scholar
  31. 31.
    Battley EH (2009) Is electron equivalence between substrate and product preferable to C-mol equivalence in representations of microbial anabolism applicable to “origin of life” environmental conditions. J Theor Biol 260(2):267–275CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lanmei Zhao
    • 1
    • 2
  • Congcong Zhang
    • 5
  • Haoshuai Li
    • 1
    • 2
  • Mutai Bao
    • 1
    • 2
    Email author
  • Peiyan Sun
    • 3
    • 4
  1. 1.Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education/Institute for Advanced Ocean StudyOcean University of ChinaQingdaoChina
  2. 2.College of Chemistry and Chemical EngineeringOcean University of ChinaQingdaoChina
  3. 3.Key Laboratory of Marine Spill Oil Identification and Damage Assessment TechnologyState Oceanic AdministrationQingdaoChina
  4. 4.North China Sea Environmental Monitoring CenterState Oceanic AdministrationQingdaoChina
  5. 5.Departament d’Enginyeria Química, Biològica i Ambiental, Escola d’EnginyeriaUniversitat Autònoma de BarcelonaBarcelonaSpain

Personalised recommendations