Skip to main content
SpringerLink
Log in

Evaluation of aerobic biodegradation of phenanthrene using Pseudomonas turukhanskensis: an optimized study

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

The ability of Pseudomonas turukhanskensis GEEL-01 to degrade the phenanthrene (PHE) was optimized by response surface methodology (RSM). Three factors as independent variables (including temperature, pH, and inoculum) were studied at 600 mg/L PHE where the highest growth of P. turukhanskensis GEEL-01 was observed. The optimum operating conditions were evaluated through the fit summary analysis, model summary statistics, fit statistics, ANOVA analysis, and model graphs. The degradation of PHE was monitored by high-performance liquid chromatography (HPLC) and the metabolites were identified by gas chromatography-mass spectrometry (GC-MS). The results showed that the correlation among independent variables with experimental and predicted responses was significant (p < 0.0001). The optimal temperature, pH, and inoculum were 30 ℃, 8, and 6 mL respectively. The HPLC peaks exhibited a reduction in PHE concentration from 600 mg/L to 4.97 mg/L with 99% degradation efficiency. The GC-MS peaks indicated that the major end products of PHE degradation were 1-Hydroxy-2-naphthoic acid, salicylic acid, phthalic acid, and catechol. This study demonstrated that the optimized parameters by RSM for P. turukhanskensis GEEL-01 could degrade PHE by phthalic and salicylic acid pathways.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The dataset used and analyzed during the current study is available from the corresponding author on reasonable request.

References

  • Abdelhaleem HAR, Zein HS, Azeiz A, Sharaf AN, Abdelhadi AA (2019) Identification and characterization of novel bacterial polyaromatic hydrocarbon-degrading enzymes as potential tools for cleaning up hydrocarbon pollutants from different environmental sources. Environ Toxicol Pharmacol 67:108–116

    Article  CAS  PubMed  Google Scholar 

  • Al-Dhabaan FA (2019) Morphological, biochemical and molecular identification of petroleum hydrocarbons biodegradation bacteria isolated from oil polluted soil in Dhahran, Saud Arabia. Saudi J Biol Sci 26:1247–1252

    Article  CAS  PubMed  Google Scholar 

  • Bakshi A, Verma AK, Dash AK (2020) Electrocoagulation for removal of phosphate from aqueous solution: statistical modeling and techno-economic study. J Clean Prod 246:118988

    Article  CAS  Google Scholar 

  • Bankole PO, Semple KT, Jeon B-H, Govindwar SP (2021) Biodegradation of fluorene by the newly isolated marine-derived fungus, Mucor irregularis strain bpo1 using response surface methodology. Ecotoxicol Environ Safety 208:111619

    Article  CAS  PubMed  Google Scholar 

  • Behera ID, Nayak M, Biswas S, Meikap BC, Sen R (2021) Enhanced biodegradation of total petroleum hydrocarbons by implementing a novel two-step bioaugmentation strategy using indigenous bacterial consortium. J Environ Manage 292:112746

    Article  CAS  PubMed  Google Scholar 

  • Bezerra MA, Santelli RE, Oliveira EP, Villar LS, Escaleira LA (2008) Response surface methodology (RSM) as a tool for optimization in analytical chemistry. Talanta 76:965–977

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Wang F, Zeng L, Li Q (2021) Bioremediation of petroleum-contaminated soil by semi-aerobic aged refuse biofilter: optimization and mechanism. J Clean Prod 294:125354

    Article  CAS  Google Scholar 

  • Ding Z, Huang J, Chi J (2021) Contribution of phenanthrene in different binding sites to its biodegradation in biochar-amended soils. Environ Pollut 273:116481

    Article  CAS  PubMed  Google Scholar 

  • Favier L, Ungureanu CV, Simion AI, Bahrim G, Vial C (2021) Enhancing the biodegradation efficiency of a emergent refractory water pollutant by a bacterial isolate through a statistical process optimization approach. Process Saf Environ Prot 148:1133–1145

    Article  CAS  Google Scholar 

  • Fu W, Xu M, Sun K, Hu L, Cao W, Dai C, Jia Y (2018) Biodegradation of phenanthrene by endophytic fungus Phomopsis liquidambari in vitro and in vivo. Chemosphere 203:160–169

    Article  CAS  PubMed  Google Scholar 

  • Gao S, Seo J-S, Wang J, Keum Y-S, Li J, Li QX (2013) Multiple degradation pathways of phenanthrene by Stenotrophomonas maltophilia C6. Int Biodeterior Biodegrad 79:98–104

    Article  CAS  Google Scholar 

  • Gu H, Yan K, You Q, Chen Y, Pan Y, Wang H, Wu L, Xu J (2021) Soil indigenous microorganisms weaken the synergy of Massilia sp. WF1 and Phanerochaete chrysosporium in phenanthrene biodegradation. Sci Total Environ 781:146655

    Article  CAS  PubMed  Google Scholar 

  • Hall B, Acar Kirit H, Nandipati A, Barlow M (2013) Growth rates made easy. Mol Biol Evol 31:232–238

    Article  PubMed  Google Scholar 

  • Hidalgo KJ, Sierra-Garcia IN, Dellagnezze BM, de Oliveira VM (2020) Metagenomic insights into the mechanisms for biodegradation of polycyclic aromatic hydrocarbons in the oil supply chain. Front Microbiol 11:561506

    Article  PubMed  PubMed Central  Google Scholar 

  • Hidayat A, Yanto DHY (2018) Biodegradation and metabolic pathway of phenanthrene by a new tropical fungus, Trametes hirsuta D7. J Environ Chem Eng 6:2454–2460

    Article  CAS  Google Scholar 

  • Hou N, Zhang N, Jia T, Sun Y, Dai Y, Wang Q, Li D, Luo Z, Li C (2018) Biodegradation of phenanthrene by biodemulsifier-producing strain Achromobacter sp. LH-1 and the study on its metabolisms and fermentation kinetics. Ecotoxicol Environ Saf 163:205–214

    Article  CAS  PubMed  Google Scholar 

  • Isaac P, Lozada M, Dionisi HM, Estévez MC, Ferrero MA (2015) Differential expression of the catabolic nahAc gene and its effect on PAH degradation in Pseudomonas strains isolated from contaminated Patagonian coasts. Int Biodeterior Biodegrad 105:1–6

    Article  CAS  Google Scholar 

  • Jia H, Zhao J, Fan X, Dilimulati K, Wang C (2012) Photodegradation of phenanthrene on cation-modified clays under visible light. Appl Catal B 123–124:43–51

    Article  Google Scholar 

  • Jiang Y, Huang H, Wu M, Yu X, Chen Y, Liu P, Li X (2015) Pseudomonas sp. LZ-Q continuously degrades phenanthrene under hypersaline and hyperalkaline condition in a membrane bioreactor system. Biophys Rep 1:156–167

    Article  CAS  PubMed  Google Scholar 

  • Kazemian A, basati Y, Khatibi M, Ma T (2021) Performance prediction and optimization of a photovoltaic thermal system integrated with phase change material using response surface method. J Clean Prod 290:125748

    Article  Google Scholar 

  • Kong J, Wang H, Liang L, Li L, Xiong G, Hu Z (2017) Phenanthrene degradation by the bacterium Pseudomonas stutzeri JP1 under low oxygen condition. Int Biodeterior Biodegrad 123:121–126

    Article  CAS  Google Scholar 

  • Li W, Zhu X, He Y, Xing B, Xu J, Brookes PC (2013) Enhancement of water solubility and mobility of phenanthrene by natural soil nanoparticles. Environ Pollut 176:228–233

    Article  CAS  PubMed  Google Scholar 

  • Lin M, Hu X, Chen W, Wang H, Wang C (2014) Biodegradation of phenanthrene by Pseudomonas sp. BZ-3, isolated from crude oil contaminated soil. Int Biodeterior Biodegrad 94:176–181

    Article  CAS  Google Scholar 

  • Lin M, Qiu R, Fu Y, Hu J, Ruan J (2021) Optimizing conditions of key factors influencing CN – producing ability of Pseudomonas biofilm to leach Ag from waste printed circuit boards. J Clean Prod 288:125641

    Article  CAS  Google Scholar 

  • Liu Y, Hu H, Zanaroli G, Xu P, Tang H (2021) A Pseudomonas sp. strain uniquely degrades PAHs and heterocyclic derivatives via lateral dioxygenation pathways. J Hazard Mater 403:123956

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Liu J, Dick RP, Li H, Shen D, Gao Y, Waigi MG, Ling W (2018) Rhamnolipid influences biosorption and biodegradation of phenanthrene by phenanthrene-degrading strain Pseudomonas sp.Ph6. Environ Pollut 240:359–367

    Article  CAS  PubMed  Google Scholar 

  • Madrid F, Rubio-Bellido M, Morillo E (2020) Extraction of nonylphenol, pyrene and phenanthrene from sewage sludge and composted biosolids by cyclodextrins and rhamnolipids. Sci Total Environ 715:136986

    Article  CAS  PubMed  Google Scholar 

  • Mang DY, Abdou AB, Njintang NY, Djiogue EJM, Loura BB, Mbofung MC (2015) Application of desirability-function and RSM to optimize antioxidant properties of mucuna milk. J Food Measure Characteriz 9:495–507

    Article  Google Scholar 

  • Mangwani N, Shukla SK, Rao TS, Das S (2014) Calcium-mediated modulation of Pseudomonas mendocina NR802 biofilm influences the phenanthrene degradation. Colloids Surf B: Biointerfaces 114:301–309

    Article  CAS  PubMed  Google Scholar 

  • Masakorala K, Yao J, Cai M, Chandankere R, Yuan H, Chen H (2013) Isolation and characterization of a novel phenanthrene (PHE) degrading strain Psuedomonas sp. USTB-RU from petroleum contaminated soil. J Hazard Mater 263 Pt 2:493–500

    Article  Google Scholar 

  • Pandya DK, Kumar MA (2021) Chemo-metric engineering designs for deciphering the biodegradation of polycyclic aromatic hydrocarbons. J Hazard Mater 411:125154

    Article  CAS  PubMed  Google Scholar 

  • Patel V, Cheturvedula S, Madamwar D (2012) Phenanthrene degradation by Pseudoxanthomonas sp. DMVP2 isolated from hydrocarbon contaminated sediment of Amlakhadi canal, Gujarat, India. J Hazard Mater 201–202:43–51

    Article  PubMed  Google Scholar 

  • Pedetta A, Pouyte K, Herrera Seitz MK, Babay PA, Espinosa M, Costagliola M, Studdert CA, Peressutti SR (2013) Phenanthrene degradation and strategies to improve its bioavailability to microorganisms isolated from brackish sediments. Int Biodeterior Biodegrad 84:161–167

    Article  CAS  Google Scholar 

  • Rabodonirina S, Rasolomampianina R, Krier F, Drider D, Merhaby D, Net S, Ouddane B (2019) Degradation of fluorene and phenanthrene in PAHs-contaminated soil using Pseudomonas and Bacillus strains isolated from oil spill sites. J Environ Manage 232:1–7

    Article  CAS  PubMed  Google Scholar 

  • Roslund MI, Grönroos M, Rantalainen A-L, Jumpponen A, Romantschuk M, Parajuli A, Hyöty H, Laitinen O, Sinkkonen A (2018) Half-lives of PAHs and temporal microbiota changes in commonly used urban landscaping materials. Peer J 6:e4508

    Article  PubMed  PubMed Central  Google Scholar 

  • She B, Tao X, Huang T, Lu G, Zhou Z, Guo C, Dang Z (2016) Effects of nano bamboo charcoal on PAHs-degrading strain Sphingomonas sp. GY2B. Ecotoxicol Environ Saf 125:35–42

    Article  CAS  PubMed  Google Scholar 

  • Singh P, Tiwary BN (2017) Optimization of conditions for polycyclic aromatic hydrocarbons (PAHs) degradation by Pseudomonas stutzeri P2 isolated from Chirimiri coal mines. Biocatal Agric Biotechnol 10:20–29

    Article  CAS  Google Scholar 

  • Sonwani RK, Kim K-H, Zhang M, Tsang YF, Lee SS, Giri BS, Singh RS, Rai BN (2021) Construction of biotreatment platforms for aromatic hydrocarbons and their future perspectives. J Hazard Mater 416:125968

    Article  CAS  PubMed  Google Scholar 

  • Sun K, Liu J, Gao Y, Jin L, Gu Y, Wang W (2014) Isolation, plant colonization potential and phenanthrene degradation performance of the endophytic bacterium Pseudomonas sp. Ph6-gfp. Sci Rep 4:5462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun S, Wang H, Chen Y, Lou J, Wu L, Xu J (2019) Salicylate and phthalate pathways contributed differently on phenanthrene and pyrene degradations in Mycobacterium sp. WY10. J Hazard Mater 364:509–518

    Article  CAS  PubMed  Google Scholar 

  • Sun S, Wang H, Fu B, Zhang H, Lou J, Wu L, Xu J (2020) Non-bioavailability of extracellular 1-hydroxy-2-naphthoic acid restricts the mineralization of phenanthrene by Rhodococcus sp. WB9. Sci Total Environ 704:135331

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Zhu B, Yang F, Dai M, Sehar S, Peng C, Ali I, Naz I (2021) Optimization of biosurfactant production from Pseudomonas sp. CQ2 and its application for remediation of heavy metal contaminated soil. Chemosphere 265:129090

    Article  CAS  PubMed  Google Scholar 

  • Suszek-Łopatka B, Maliszewska-Kordybach B, Klimkowicz-Pawlas A, Smreczak B (2016) Influence of temperature on phenanthrene toxicity towards nitrifying bacteria in three soils with different properties. Environ Pollut 216:911–918

    Article  PubMed  Google Scholar 

  • Tao X-Q, Lu G-N, Dang Z, Yi X-Y, Yang C (2007) Isolation of phenanthrene-degrading bacteria and characterization of phenanthrene metabolites. World J Microbiol Biotechnol 23:647–654

    Article  CAS  Google Scholar 

  • Tsai J-C, Kumar M, Chang S-M, Lin J-G (2009) Determination of optimal phenanthrene, sulfate and biomass concentrations for anaerobic biodegradation of phenanthrene by sulfate-reducing bacteria and elucidation of metabolic pathway. J Hazard Mater 171:1112–1119

    Article  CAS  PubMed  Google Scholar 

  • Turkovskaya O, Muratova A (2019) Plant–bacterial degradation of polyaromatic hydrocarbons in the Rhizosphere. Trends Biotechnol 37:926–930

    Article  CAS  PubMed  Google Scholar 

  • Uslu S (2020) Optimization of diesel engine operating parameters fueled with palm oil-diesel blend: comparative evaluation between response surface methodology (RSM) and artificial neural network (ANN). Fuel 276:117990

    Article  CAS  Google Scholar 

  • Vijayalakshmi V, Senthilkumar P, Mophin-Kani K, Sivamani S, Sivarajasekar N, Vasantharaj S (2018) Bio-degradation of bisphenol A by Pseudomonas aeruginosa PAb1 isolated from effluent of thermal paper industry: kinetic modeling and process optimization. J Radiat Res Appl Sci 11:56–65

    Article  CAS  Google Scholar 

  • Wang P, Zhang Y, Jin J, Wang T, Wang J, Jiang B (2020) A high-efficiency phenanthrene-degrading Diaphorobacter sp. isolated from PAH-contaminated river sediment. Sci Total Environ 746:140455

    Article  CAS  PubMed  Google Scholar 

  • Wu ML, Nie MQ, Wang XC, Su JM, Cao W (2010) Analysis of phenanthrene biodegradation by using FTIR, UV and GC–MS. Spectrochimica Acta Part A: Mol Biomol Spectro 75:1047–1050

    Article  CAS  Google Scholar 

  • Xu X, Li H, Wang Q, Li D, Han X, Yu H (2017) A facile approach for surface alteration of Pseudomonas putida I3 by supplying K2SO4 into growth medium: enhanced removal of Pb(II) from aqueous solution. Bioresour Technol 232:79–86

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Liu W, Wang W, Tian S, Jiang P, Qi Q, Li F, Li H, Wang Q, Li H, Yu H (2019) Potential biodegradation of phenanthrene by isolated halotolerant bacterial strains from petroleum oil polluted soil in Yellow River Delta. Sci Total Environ 664:1030–1038

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Chen Z, Wu Q, Xu M (2018) Enhanced phenanthrene degradation in river sediments using a combination of biochar and nitrate. Sci Total Environ 619–620:600–605

    Article  PubMed  Google Scholar 

  • Zhang D, Han X, Zhou S, Yuan S, Lu P, Peng S (2021) Nitric oxide-dependent biodegradation of phenanthrene and fluoranthene: the co-occurrence of anaerobic and intra-aerobic pathways. Sci Total Environ 760:144032

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Zhang Y, Xiao X, Li G, Zhao Y, Liang Y (2017) Different phenanthrene-degrading bacteria cultured by in situ soil substrate membrane system and traditional cultivation. Int Biodeterior Biodegrad 117:269–277

    Article  CAS  Google Scholar 

  • Zeng J, Zhu Q, Li Y, Dai Y, Wu Y, Sun Y, Miu L, Chen H, Lin X (2019): Isolation of diverse pyrene-degrading bacteria via introducing readily utilized phenanthrene. Chemosphere 222, 534-540

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by a start-up fund for the “Construction of the double first-class” project (grant number 561119201), Lanzhou University, China. This work was also supported by National Natural Science Foundation (No. 32070117, 31870082).

Author information

Authors and Affiliations

  1. MOE, Key Laboratory of Cell Activities and Stress Adaptations, Lanzhou University, Lanzhou, 730000, Gansu Province, PR China

    Monika Sharma, Muhammad Usman, Aman Khan, Muhammad Arif & Xiangkai Li

  2. Department of Occupational and Environmental Health, School of Public Health, Lanzhou University, Lanzhou, 730000, Gansu Province, PR China

    Monika Sharma, El-Sayed Salama, Muhammad Usman & Muhammad Arif

Authors
  1. Monika Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. El-Sayed Salama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Usman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aman Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Arif
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiangkai Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MS: Methodology, Visualization, Investigation, Data curation, Formal analysis, Writing, Original Draft. E-SS: Conceptualization, Supervision, Resources, Data Curation, Validation, Visualization, Formal analysis, Writing - Review & Editing, Funding acquisition, Project administration. MU: Formal analysis, Editing. AK: Visualization, Formal analysis. MA: Visualization, Formal analysis. XL: Supervision, Resources, Data Curation, Validation, Funding acquisition, Project administration.

Corresponding authors

Correspondence to El-Sayed Salama or Xiangkai Li.

Ethics declarations

Competing interests

The authors declare no competing interest.

Ethical approval

Not applicable.

Consent for publication

All the authors agree to publish this article.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1227 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, M., Salama, ES., Usman, M. et al. Evaluation of aerobic biodegradation of phenanthrene using Pseudomonas turukhanskensis: an optimized study. Biodegradation 34, 21–41 (2023). https://doi.org/10.1007/s10532-022-10002-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-022-10002-5

Keywords

Search

Navigation