Skip to main content
SpringerLink
Log in

Biodegradation capabilities of filamentous fungi in high-concentration heavy crude oil environments

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

In this comprehensive study, we delved into the capabilities of five fungal strains: Aspergillus flavus, Aspergillus niger, Penicillium chrysogenum, Penicillium glabrum, and Penicillium rubens (the latter isolated from heavy crude oil [HCO]) in metabolizing HCO as a carbon source. Employing a meticulously designed experimental approach, conducted at room temperature (25 °C), we systematically explored various culture media and incubation periods. The results unveiled the exceptional resilience of all these fungi to HCO, with A. flavus standing out as the top performer. Notably, A. flavus exhibited robust growth, achieving a remarkable 59.1% expansion across the medium’s surface, accompanied by distinctive macroscopic traits, including a cottony appearance and vibrant coloration. In an effort to further scrutinize its biotransformation prowess, we conducted experiments in a liquid medium, quantifying CO2 production through gas chromatography, which reached its zenith at day 30, signifying substantial bioconversion with a 38% increase in CO2 production. Additionally, we monitored changes in surface tension using the Du Noüy ring method, revealing a reduction in aqueous phase tension from 72.3 to 47 mN/m. This compelling evidence confirms that A. flavus adeptly metabolizes HCO to fuel its growth, while concurrently generating valuable biosurfactants. These findings underscore the immense biotechnological potential of A. flavus in addressing challenges related to HCO, thereby offering promising prospects for bioremediation and crude oil bioupgrading endeavors.

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

References

  • Al-Dossary MA, Abood SA, Al-Saad HT (2020) Factors affecting polycyclic aromatic hydrocarbon biodegradation by Aspergillus flavus. Remediat J 30(4):17–25

    Article  Google Scholar 

  • Al-Hawash AB, Dragh MA, Li S, Alhujaily A, Abbood HA, Zhang X, Ma F (2018) Principles of microbial degradation of petroleum hydrocarbons in the environment. Egyptian J Aqu Res 44(2):71–76

    Article  Google Scholar 

  • Amran RH, Jamal MT, Pugazhendi A, Al-Harbi M, Ghandourah M, Al-Otaibi A, Haque MF (2022) Biodegradation and bioremediation of petroleum hydrocarbons in marine ecosystems by microorganisms: a review. Nat Environ Pollut Technol 21(3):1149–1157

    Article  CAS  Google Scholar 

  • Araujo J, Yegres F, Barreto G, Antequera AA, Depool B, Rojas Y (2016) Biocatalizadores fúngicos hidrocarbonoclásticos del género Aspergillus para la descontaminación de agua con Hidrocarburos Policíclicos Aromáticos (HPAs). Revista Cubana De Química 28(2):703–735

    Google Scholar 

  • Aydin S, Karacay HA, Shahi A, Gokce S, Ince B, Ince O (2017) Aerobic and anaerobic fungal metabolism and Omics insights for increasing polycyclic aromatic hydrocarbons biodegradation. Fungal Biol Rev 31:61–72

    Article  Google Scholar 

  • Ayala M, Hernandez-Lopez EL, Perezgasga L, Vazquez-Duhalt R (2012) Reduced coke formation and aromaticity due to chloroperoxidase-catalyzed transformation of asphaltenes from Maya crude oil. Fuel 92(1):245–249

    Article  CAS  Google Scholar 

  • Barbedo JGA (2013) Automatic object counting in Neubauer chambers

  • Borole AP, Ramirez-Corredores MM (2007) Biocatalysis in oil refining. Oak Ridge National Lab (ORNL), Oak Ridge, TN

  • Carrillo L (2003) Los hongos de los alimentos y forrajes. Universidad Nacional De Salta, Argentina 118:20

    Google Scholar 

  • Carrillo L, Audisio MC, Bejarano N, Gómez S, Ancasi G, Benítez M (2007) Manual de Microbiología de los Alimentos. Jujuy 10:102–116

    Google Scholar 

  • Castro LV, Vazquez F (2009) Fractionation and characterization of Mexican crude oils. Energy Fuels 23(3):1603–1609

    Article  CAS  Google Scholar 

  • Central Intelligence Agency (2018) Crude oil—proved reserves. https://www.cia.gov/the-world-factbook/field/crude-oil-proved-reserves/country-comparison

  • Chen W, Kong Y, Li J, Sun Y, Min J, Hu X (2020) Enhanced biodegradation of crude oil by constructed bacterial consortium comprising salt-tolerant petroleum degraders and biosurfactant producers. Int Biodeterio Biodegrad 154:105047

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Demirbas A, Bafail A, Nizami A (2016) Heavy oil upgrading: unlocking the future fuel supply. Pet Sci Technol 34(4):303–308

    Article  CAS  Google Scholar 

  • Durand E, Clemancey M, Lancelin JJ, Verstraete J, Espinat D, Quoineaud AA (2010) Effect of chemical composition on asphaltenes aggregation. Energy Fuels 24:1051–1062

    Article  CAS  Google Scholar 

  • El-Gendy NS, Speight JG (2015) Handbook of refinery desulfurization (Vol. 140). CRC Press

  • Elshafie A, AlKindi YA, Al-Busaidi S, Bakheit C, Albahry SN (2007) Biodegradation of crude oil and n-alkanes by fungi isolated from Oman. Mar Pollut Bull 54:1692–1696

    Article  PubMed  CAS  Google Scholar 

  • El-Shall H, Abu Serie M, Abu-Elreesh G, Eltarahony M (2023) Unveiling the anticancer potentiality of single cell oils produced by marine oleaginous Paradendryphiella sp. under optimized economic growth conditions. Sci Rep 13(1):20773

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  • Fida TT, Chen C, Okpala G, Voordouw G (2016) Implications of limited thermophilicity of nitrite reduction for control of sulfide production in oil reservoirs. Appl Environ Microbiol 82(14):4190–4199

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  • Foght JM (2004) Whole-cell bio-processing of aromatic compounds in crude oil and fuels. In Studies in surface science and catalysis (Vol. 151, pp. 145-175). Elsevier

  • Gargouri B, Contreras MM, Ammar S et al (2017) Biosurfactant production by the crude oil degrading Stenotrophomonas sp. B-2: chemical characterization, biological activities and environmental applications. Environ Sci Pollut Res 24:3769–3779. https://doi.org/10.1007/s11356-016-8064-4

    Article  CAS  Google Scholar 

  • Graus W, Roglieri M, Jaworski P, Alberio L, Worrell E (2011) The promise of carbon capture and storage: evaluating the capture-readiness of new EU fossil fuel power plants. Clim Policy 11:789–812

    Article  Google Scholar 

  • Gudiña EJ, Teixeira JA (2017) HC-0C-03: Biological treatments to improve the quality of heavy crude oils. In: Biodegradation and bioconversion of hydrocarbons, pp 337–351

  • Gudiña EJ, Pereira JF, Rodrigues LR, Coutinho JA, Teixeira JA (2012) Isolation and study of microorganisms from oil samples for application in microbial enhanced oil recovery. Int Biodeterior Biodegradation 68:56–64

    Article  Google Scholar 

  • Gudiña EJ, Pereira JF, Costa R, Coutinho JA, Teixeira JA, Rodrigues LR (2013a) Biosurfactant-producing and oil-degrading Bacillus subtilis strains enhance oil recovery in laboratory sand-pack columns. J Hazard Mater 261:106–113

    Article  PubMed  Google Scholar 

  • Gudiña EJ, Pereira JF, Costa R, Rodrigues LR, Coutinho JA, Teixeira JA (2013b) A biosurfactantproducing and oil-degrading Bacillus subtilis strain enhances oil recovery under simulated reservoir conditions.https://hdl.handle.net/1822/28708

  • Head IM, Jones DM, Larter SR (2003) Biological activity in the deep subsurface and the origin of heavy oil. Nature 426(6964):344–352

    Article  PubMed  ADS  CAS  Google Scholar 

  • Harner NK, Richardson TL, Thompson KA, Best RJ, Best AS, Trevors JT (2011) Microbial processes in the Athabasca Oil Sands and their potential applications in microbial enhanced oil recovery. J Indus Microbiol Biotechnol 38(11):1761

    Article  PubMed  CAS  Google Scholar 

  • Hare JM (2013) Sabouraud agar for fungal growth. In: Laboratory protocols in fungal biology. Springer, New York, pp 211–216

  • Heimann K, Muthu SS, Karthikeyan OP (2017) Biodegradation and bioconversion of hydrocarbons. Springer, Singapore

    Book  Google Scholar 

  • Hernández-López EL, Ayala M, Vazquez-Duhalt R (2015) Microbial and enzymatic biotransformations of asphaltenes. Pet Sci Technol 33(9):1017–1029

    Article  Google Scholar 

  • Hernández-López EL, Perezgasga L, Huerta-Saquero A, Mouriño-Pérez R, Vazquez-Duhalt R (2016) Biotransformation of petroleum asphaltenes and high molecular weight polycyclic aromatic hydrocarbons by Neosartorya fischeri. Environ Sci Pollut Res 23(11):10773–10784

    Article  Google Scholar 

  • He L, Lin F, Li X, Sui H, Xu Z (2015) Interfacial sciences in unconventional petroleum production: from fundamentals to applications. Chem Soc Rev 44(15):5446–5494

    Article  PubMed  CAS  Google Scholar 

  • Hildebrand EM (1938) Techniques for the isolation of single microorganisms. Bot Rev 4(12):627–664

    Article  Google Scholar 

  • IEA (2019) World Energy Outlook 2019. IEA, Paris. https://www.iea.org/reports/world-energy-outlook-2019

  • Ismail W, El Nayal AM, Ramadan AR, Abotalib N (2014) Sulfur source-mediated transcriptional regulation of the rhlABC genes involved in biosurfactants production by Pseudomonas sp. strain AK6U. Front Microbiol 5:423. https://doi.org/10.3389/fmicb.2014.00423

    Article  PubMed  PubMed Central  Google Scholar 

  • Ismail WA, Mohamed MES, Awadh MN, Obuekwe C, El Nayal AM (2017a) Simultaneous valorization and biocatalytic upgrading of heavy vacuum gas oil by the biosurfactant-producing Pseudomonas aeruginosa AK6U. Microb Biotechnol 10(6):1628–1639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ismail WA, Van Hamme JD, Kilbane JJ, Gu JD (2017b) Petroleum microbial biotechnology: challenges and prospects. Front Microbiol 8:833

    Article  PubMed  PubMed Central  Google Scholar 

  • Ismail WA, Mohamed MES, Awadh MN, Obuekwe C, El Nayal AM (2017) Simultaneous valorization and biocatalytic upgrading of heavy vacuum gas oil by the biosurfactant-producing Pseudomonas aeruginosa AK6U. Microbial Biotechnol 10(6):1628–1639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jasalavich CA, Ostrofsky A, Jellison J (2000) Detection and identification of decay fungi in spruce wood by restriction fragment length polymorphism analysis of amplified genes encoding rRNA. Appl Environ Microbiol 66(11):4725–4734

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  • Leon V, Kumar M (2005) Biological upgrading of heavy crude oil. Biotechnol Bioprocess Eng 10(6):471–481

    Article  CAS  Google Scholar 

  • Martínez-Martín E, Acosta-Martínez L, Ramírez-Apodaca FD (2016) Crude oil emulsification for pipeline transportation. Ing Investig Tecnol 17(3):395–403

    Google Scholar 

  • Madden PB, Morawski JD (2011) The future of the canadian oil stands: engineering and project management advances. Energy Environ 22(5):579–596

    Article  Google Scholar 

  • Mirchi A, Hadian S, Madani K, Rouhani OM, Rouhani AM (2012) World energy balance outlook and OPEC production capacity: implications for global oil security. Energies 5(8):2626–2651

    Article  Google Scholar 

  • Mnif S, Chamkha M, Labat M, Sayadi S (2011) Simultaneous hydrocarbon biodegradation and biosurfactant production by oilfield-selected bacteria. J Appl Microbiol 111:525–536

    Article  PubMed  CAS  Google Scholar 

  • Naranjo L, Urbina H, De Sisto A, Leon V (2007) Isolation of autochthonous non-white rot fungi with potential for enzymatic upgrading of Venezuelan extra-heavy crude oil. Biocatal Biotransform 25(2–4):341–349

    Article  CAS  Google Scholar 

  • Nikolova C, Gutierrez T (2020) Use of microorganisms in the recovery of oil from recalcitrant oil reservoirs: current state of knowledge, technological advances and future perspectives. Front Microbiol 10:2996

    Article  PubMed  PubMed Central  Google Scholar 

  • Olivera NL, Nievas ML, Lozada M, Del Prado G, Dionisi HM, Siñeriz F (2009) Isolation and characterization of biosurfactant-producing Alcanivorax strains: hydrocarbon accession strategies and alkane hydroxylase gene analysis. Research in microbiology 160(1):19–26

    Article  PubMed  CAS  Google Scholar 

  • Rana MS, Sámano V, Ancheyta J, Diaz JAI (2007) A review of recent advances on process technologies for upgrading of heavy oils and residua. Fuel 86(9):1216–1231

    Article  CAS  Google Scholar 

  • She YH, Zhang F, Xia JJ, Kong SQ, Wang ZL, Shu FC, Hu JM (2011) Investigation of biosurfactant-producing indigenous microorganisms that enhance residue oil recovery in an oil reservoir after polymer flooding. Appl Biochem Biotechnol 163(2):223–234

    Article  PubMed  CAS  Google Scholar 

  • Shibulal B, Al-Bahry SN, Al-Wahaibi YM, Elshafie AE, Al-Bemani AS, Joshi SJ (2014) Microbial enhanced heavy oil recovery by the aid of inhabitant spore-forming bacteria: an insight review. ScientificWorldJournal 2014:309159

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh NK, Choudhary S (2021) Bacterial and archaeal diversity in oil fields and reservoirs and their potential role in hydrocarbon recovery and bioprospecting. Environ Sci Pollut Res 28:58819–58836. https://doi.org/10.1007/s11356-020-11705-z

    Article  CAS  Google Scholar 

  • Soberón-Chávez G, Maier RM (2011) Biosurfactants: a general overview. In: Soberón-Chávez G (ed) Biosurfactants: from genes to applications. Springer, Berlin, pp 1–11

    Chapter  Google Scholar 

  • Speight JG (2014) The chemistry and technology of crude oil, 5th edn. CRC Press, Boca Raton, FL

    Google Scholar 

  • Speight JG (2017) Handbook of petroleum refining. CRC Press, Boca Raton, FL

    Google Scholar 

  • Speight JG (2019) Heavy oil recovery and upgrading. Gulf Professional Publishing, Cambridge, MA

    Google Scholar 

  • Speight JG, El-Gendy NS (2017) Introduction to petroleum biotechnology. Gulf Professional Publishing, Cambridge, MA

    Google Scholar 

  • Strubinger A, Ehrmann U, León V, DeSisto A, González M (2015) Changes in Venezuelan Orinoco belt crude after different biotechnological approaches. J Petrol Sci Eng 127:421–432

    Article  CAS  Google Scholar 

  • Sugai Y, Komatsu K, Sasaki K, Mogensen K, Bennetzen MV (2014) Microbial-induced oil viscosity reduction by selective degradation of long-chain alkanes. In: Abu Dhabi International Petroleum Exhibition and Conference. OnePetro

  • Tavassoli T, Mousavi SM, Shojaosadati SA, Salehizadeh H (2012) Asphaltene biodegradation using microorganisms isolated from oil samples. Fuel 93:142–148

    Article  CAS  Google Scholar 

  • Uribe-Alvarez C, Ayala M, Perezgasga L, Naranjo L, Urbina H, Vazquez-Duhalt R (2011) First evidence of mineralization of petroleum asphaltenes by a strain of Neosartorya fischeri. Microb Biotechnol 4(5):663–672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Varjani SJ, Patel RK (2017) Fungi: a remedy to eliminate environmental pollutants. Mycoremediat Environ Sustain 1:53–67

    Article  Google Scholar 

  • Walter V, Syldatk C, Hausmann R (2010) Biosurfactants: screening concepts for the isolation of biosurfactant producing microorganisms. Adv Exp Med Biol 672:1–13. https://doi.org/10.1007/978-1-4419-5979-9_1

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Tang Y, Wang S, Liu RL, Liu MZ, Zhang Y et al (2006) Isolation and characterization of a novel thermophilic Bacillus strain degrading long-chain n-alkanes. Extremophiles 10(4):347–356

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Wu S, Cui J, Yu X, Zhang H (2020) Determination of wax removal and viscosity reduction in crude oil treated by dominant bacteria. Pet Sci Technol 38(7):627–634

    Article  CAS  Google Scholar 

  • Ward OP (2010) Microbial biosurfactants and biodegradation. Adv Exp Med Biol 672:65–74

    Article  PubMed  CAS  Google Scholar 

  • Yanto DHY, Tachibana S (2013) Biodegradation of petroleum hydrocarbons by a newly isolated Pestalotiopsis sp. NG007. Int Biodeterior Biodegradation 85:438–450

    Article  CAS  Google Scholar 

  • Yanto DHY, Tachibana S (2014) Potential of fungal co-culturing for accelerated biodegradation of petroleum hydrocarbons in soil. J Hazard Mater 278:454–463

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We extend our sincere gratitude to the Agencia Nacional de Investigación y Desarrollo (ANID), for generously funding this research project. We also wish to express our appreciation to the Pontificia Universidad Católica de Chile (PUC) and the Empresa Nacional del Petróleo de Chile (ENAP) for their invaluable contributions in providing the heavy crude oil samples that were instrumental in making this study a reality. Their support and collaboration were indispensable to the success of this research endeavor.

Funding

This work was supported by the Chilean national research and development agency ANID, through the covenant 3617/2021.

Author information

Authors and Affiliations

  1. Doctorado en Ciencias de La Ingeniería, Departamento de Ingeniería Química y Bioprocesos, Escuela de Ingeniería, Pontificia Universidad Católica de Chile, Avenida Vicuña Mackenna 4860, Macul, 7820436, Santiago, Macul, Chile

    Jessica Zerimar Cáceres-Zambrano & Yoandy Coca Rives

  2. Escuela de Ingeniería, Facultad de Ingeniería, Universidad Santo Tomás, Avenida Ejército Libertador 146, Santiago, Región Metropolitana, Chile

    Leonardo Andrés Rodríguez-Córdova

  3. Departamento de Ingeniería Química y Bioprocesos, Pontificia Universidad Católica de Chile, Avenida Vicuña Mackenna 4860, Macul, 7820436, Santiago, Región Metropolitana, Chile

    César Antonio Sáez-Navarrete

  4. Centro de Investigación en Nanotecnología y Materiales Avanzados (CIEN-UC), Pontificia Universidad Católica de Chile, Avenida Vicuña Mackenna 4860, Macul, 7820436, Santiago, Región Metropolitana, Chile

    César Antonio Sáez-Navarrete

Authors
  1. Jessica Zerimar Cáceres-Zambrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonardo Andrés Rodríguez-Córdova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. César Antonio Sáez-Navarrete
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoandy Coca Rives
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception and design of the study. JZC-Z prepared the materials, collected and analyzed the data, performed the experiments, and wrote the first draft. LAR-C and CAS-N were responsible for the adaptation and improvement of the methodology, as well as the supervision of the inputs. YCR checked the data graphics and statistical analysis. All authors commented on earlier versions of the manuscript and read and approved the final manuscript.

Corresponding author

Correspondence to Jessica Zerimar Cáceres-Zambrano.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Communicated by Yusuf Akhter.

Publisher's Note

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

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

Cáceres-Zambrano, J.Z., Rodríguez-Córdova, L.A., Sáez-Navarrete, C.A. et al. Biodegradation capabilities of filamentous fungi in high-concentration heavy crude oil environments. Arch Microbiol 206, 123 (2024). https://doi.org/10.1007/s00203-024-03835-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-024-03835-6

Keywords

Search

Navigation