OpenLB
Open Library of Bioscience
Advanced Search
World journal of microbiology & biotechnology
Oct 03, 2024;40 (11): 336.

Bioremediation petroleum wastewater and oil-polluted soils by the non-toxigenic indigenous fungi.

Fuad Ameen, Mohammad J Alsarraf, Steven L Stephenson
Author Information
  1. Fuad Ameen: Department of Botany & Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia. fuadameen@ksu.edu.sa. ORCID
  2. Mohammad J Alsarraf: Department of Science, College of Basic Education, The Public Authority of Applied Education and Training (PAAET), P.O. Box 23167, 13092, Safat, Kuwait.
  3. Steven L Stephenson: Department of Biological Sciences, University of Arkansas, Fayetteville, AR, USA.
PMID: 39358660 DOI: 10.1007/s11274-024-04146-0

Abstract

Soil and wastewater samples contaminated by petroleum-related industries were collected from various locations in Saudi Arabia, a country known for its vast oil reserves. The samples were analyzed for their physicochemical properties, including the presence of metals, petroleum hydrocarbons, and aromatic compounds. A total of 264 fungal isolates were analyzed and categorized into eight groups of Aspergillus (194 isolates) and four groups of Penicillium (70 isolates). The potential of these fungal groups to grow in oil or its derivatives was investigated. Two isolates, Aspergillus tubingensis FA-KSU5 and A. niger FU-KSU69, were utilized in two remediation experiments-one targeting wastewater and the other focusing on polluted soil. The FA-KSU5 strain demonstrated complete removal of Fe, As, Cr, Zn, Mn, Cu and Cd, with bioremediation efficiency for petroleum hydrocarbons in the wastewater from these sites ranging between 90.80 and 98.58%. Additionally, the FU-KSU69 strain achieved up to 100% reduction of Co, Ba, B, V, Ni, Pb and Hg, with removal efficiency ranging from 93.17 to 96.02% for aromatic hydrocarbons after 180 min of wastewater treatment. After 21 days of soil incubation with Aspergillus tubingensis FA-KSU5, there was a 93.15% to 98.48% reduction in total petroleum hydrocarbons (TPHs) and an 88.11% to 97.31% decrease in polycyclic aromatic hydrocarbons (PAHs). This strain exhibited the highest removal rates for Cd and As followed by Fe, Zn, Cr, Se and Cu. Aspergillus niger FU-KSU69 achieved a 90.37% to 94.90% reduction in TPHs and a 95.13% to 98.15% decrease in PAHs, with significant removal of Ni, Pb and Hg, followed by Co, V, Ba and B. The enzymatic activity in the treated soils increased by 1.54- to 3.57-fold compared to the polluted soil. Although the mixture of wastewater and polluted soil exhibited high cytotoxicity against normal human cell lines, following mycoremediation, all treated soils and effluents with the dead fungal biomass showed no toxicity against normal human cell lines at concentrations up to 500 ��L/mL, with IC values���������1000 ��L/mL. SEM and IR analysis revealed morphological and biochemical alterations in the biomass of A. tubingensis FA-KSU5 and A. niger FA-KSU69 when exposed to petroleum effluents. This study successfully introduces non-toxigenic and environmentally friendly fungal strains play a crucial role in the bioremediation of contaminated environments. Both strains serve as low-cost and effective adsorbents for bio-remediating petroleum wastewater and oil-contaminated soil. Heavy metals and hydrocarbons, the primary pollutants, were either completely removed or reduced to permissible levels according to international guidelines using the dead biomass of FA-KSU5 and FA-KSU69 fungi. Consequently, the environments associated with this globally significant industry are rendered biologically safe, particularly for humans, as evidenced by the absence of cytotoxicity in samples treated with A. tubingensis FA-KSU5 and A. niger FA-KSU69 on various human cell types.

Keywords

Bioremediation Cell lines Fungi Heavy metals Petroleum wastewater Polluted soil SEM and IR analysis

References

  1. Abena BMT, Chen G, Chen Z et al (2020) Microbial diversity changes and enrichment of potential petroleum hydrocarbon degraders in crude oil-, diesel-, and gasoline-polluted soil. 3Biotech 10:42. https://doi.org/10.1007/s13205-019-2027-7 [DOI: 10.1007/s13205-019-2027-7]
  2. Ahmadi M, Akhbarizadeh R, Haghighifard NJ, Barzegar G, Jorfi S (2019) Geochemical determination and pollution assessment of heavy metals in agricultural soils of south western of Iran. J Environ Health Sci Eng 17(2):657���669. https://doi.org/10.1007/s40201-019-00379-6 [DOI: 10.1007/s40201-019-00379-6]
  3. Al-Dhabaan FA (2021) Mycoremediation of crude oil polluted soil by specific fungi isolated from Dhahran in Saudi Arabia. Saudi J Biol Sci 28(1):73���77. https://doi.org/10.1016/j.sjbs.2020.08.033 [DOI: 10.1016/j.sjbs.2020.08.033]
  4. Al-Hawash AB, Alkooranee JT, Abbood HA, Zhang J, Sun J, Zhang X, Ma F (2018) Isolation and characterization of two crude oil-degrading fungi strains from Rumaila oil field Iraq. Biotechnol Rep 17:104���109. https://doi.org/10.1016/j.btre.2017.12.006 [DOI: 10.1016/j.btre.2017.12.006]
  5. Al-Hawash AB, Zhang X, Ma F (2019) Removal and biodegradation of different petroleum hydrocarbons using the filamentous fungus Aspergillus sp. RFC-1. Microbiol Open 8:e619. https://doi.org/10.1002/mbo3.619 [DOI: 10.1002/mbo3.619]
  6. Ameen F, Moslem M, Hadi S, Al-Sabri AE (2016) Biodegradation of diesel fuel hydrocarbons by mangrove fungi from Red Sea Coast of Saudi Arabia. Saudi J Biol Sci 23:211���218. https://doi.org/10.1016/j.sjbs.2015.04.005 [DOI: 10.1016/j.sjbs.2015.04.005]
  7. Ameen F, Alsarraf MJ, Abalkhail T, Stephenson SL (2024) Evaluation of resistance patterns and bioremoval efficiency of hydrocarbons and heavy metals by the mycobiome of petroleum refining wastewater in Jazan with assessment of molecular typing and cytotoxicity of Scedosporium apiospermum JAZ-20. Heliyon 10:e32954. https://doi.org/10.1016/j.heliyon.2024.e32954 [DOI: 10.1016/j.heliyon.2024.e32954]
  8. Aniyikaiye TE, Oluseyi T, Odiyo JO, Edokpayi JN (2019) Physico-chemical analysis of wastewater discharge from selected paint industries in Lagos, Nigeria. Int J Environ Res Public Health 16:1235. https://doi.org/10.3390/ijerph16071235 [DOI: 10.3390/ijerph16071235]
  9. APHA (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington
  10. APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association and Water Environmental Federation, Washington
  11. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, Federation, Water Environmental, Washington
  12. Asemoloye MD, Tosi S, Dacc�� C, Wang X, Xu S, Marchisio MA, Gao W et al (2020) Hydrocarbon degradation and enzyme activities of Aspergillus oryzae and Mucor irregularis isolated from Nigerian crude oil-polluted sites. Microorganisms 8:1912. https://doi.org/10.3390/microorganisms8121912 [DOI: 10.3390/microorganisms8121912]
  13. Awad MF, El-Shenawy FS, El-Gendy MMAA et al (2021) Purification, characterization, and anticancer and antioxidant activities of L-glutaminase from Aspergillus versicolor Faesay4. Int Microbiol 24:169���181. https://doi.org/10.1007/s10123-020-00156-8 [DOI: 10.1007/s10123-020-00156-8]
  14. Bankole PO, Semple KT, Jeon BH et al (2020) Enhanced enzymatic removal of anthracene by the mangrove soil-derived fungus, Aspergillus sydowii BPOI. Front Environ Sci Eng 14:113. https://doi.org/10.1007/s11783-020-1292-3 [DOI: 10.1007/s11783-020-1292-3]
  15. Borowik A, Wyszkowska J, Oszust K (2017) Functional diversity of fungal communities in soil polluted with diesel oil. Front Microbiol 8:1862. https://doi.org/10.3389/fmicb.2017.01862 [DOI: 10.3389/fmicb.2017.01862]
  16. Borowik A, Wyszkowska J, Ga����zka A, Kucharski J (2019) Role of Festuca rubra and Festuca arundinacea in determining the functional and genetic diversity of microorganisms and of the enzymatic activity in the soil polluted with diesel oil. Environ Sci Pollut Res Int 26(27):27738���27751. https://doi.org/10.1007/s11356-019-05888-3 [DOI: 10.1007/s11356-019-05888-3]
  17. Camenzind T, Lehmann A, Ahland J, Rillig MC (2020) Trait-based approaches reveal fungal adaptations to nutrient-limiting conditions: fungal trait adaptations to nutrient limitations. Environ Microbiol 22(8):3548���3560. https://doi.org/10.1111/1462-2920.15132 [DOI: 10.1111/1462-2920.15132]
  18. Chanda A, Gummadidala PM, Gomaa OM (2016) Mycoremediation with mycotoxin producers: a critical perspective. Appl Microbiol Biotechnol 100:17���29. https://doi.org/10.1007/s00253-015-7032-0 [DOI: 10.1007/s00253-015-7032-0]
  19. Chaziejev FCH (1976) Fermentation activity of soils. Nauka, Moskva, pp 106���120.
  20. Claudio GJ, Vendruscolo F, Piaia JCZ, Rodrigues RC, Durrant LR, Costa JAV (2004) Radial growth rate as a tool for the selection of filamentous fungi for use in bioremediation. Braz Arch Biol Technol 47(5):35���40
  21. De Hoog GS, Guarro J, Gen�� J, Figueras MJ (2014) Atlas of cinical fungi. Webmaster Atlas, Utrecht, pp 34���37
  22. Dickson UJ, Coffey M, Mortimer RJG, Di Bonito M, Ray N (2019) Mycoremediation of petroleum contaminated soils: progress, prospects and perspectives. Environ Sci Process Impacts 21:1446���1458. https://doi.org/10.1039/C9EM00101H [DOI: 10.1039/C9EM00101H]
  23. Dindar E, ��a��ban FOT, Ba��kaya HS (2015) Variations of soil enzyme activities in petroleum-hydrocarbon polluted soil. Int Biodeterior Biodegrad 105:268���275. https://doi.org/10.1016/j.ibiod.2015.09.011 [DOI: 10.1016/j.ibiod.2015.09.011]
  24. Eaton AD, Clesceri LS, Rice EW, Greenberg AE (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association (APHA) Press, Washington
  25. El-Bondkly AMA, El-Gendy MMAA (2022) Bioremoval of some heavy metals from aqueous solutions by two different indigenous fungi Aspergillus sp. AHM69 and Penicillium sp. AHM96 isolated from petroleum refining wastewater. Heliyon 8(7):e09854. https://doi.org/10.1016/j.heliyon.2022.e09854 [DOI: 10.1016/j.heliyon.2022.e09854]
  26. El-Bondkly AAM, El-Gendy MMAA, El-Bondkly AMA (2021) Construction of efficient recombinant strain through genome shuffling in marine endophytic Fusarium sp. ALAA-20 for improvement lovastatin production using agro-industrial wastes. Arab J Sci Eng 46:175���190. https://doi.org/10.1007/s13369-020-04925-5 [DOI: 10.1007/s13369-020-04925-5]
  27. El-Gendy MMA, El-Bondkly AMA, Yahya SMM (2014) Production and evaluation of antimycotic and antihepatitis C virus potential of fusant MERV6270 derived from mangrove endophytic fungi using novel substrates of agroindustrial wastes. Appl Biochem Biotechnol 174:2674���2701. https://doi.org/10.1007/s12010-014-1218-2 [DOI: 10.1007/s12010-014-1218-2]
  28. El-Gendy MMAA, Hassanein NM, Abd El-Hay IH, Abd El-Baky DH (2017) Heavy metals biosorption from aqueous solution by endophytic Drechslera hawaiiensis of Morus alba L. derived from heavy metals habitats. Mycobiology 45(2):73���83. https://doi.org/10.5941/MYCO.2017.45.2.73 [DOI: 10.5941/MYCO.2017.45.2.73]
  29. El-Gendy MMAA, Yahya SMM, Hamed AR, Soltan MM, El-Bondkly AMA (2018) Phylogenetic analysis and biological evaluation of marine endophytic fungi derived from Red Sea sponge Hyrtios erectus. Appl Biochem Biotechnol 185(3):755���777. https://doi.org/10.1007/s12010-017-2679-x [DOI: 10.1007/s12010-017-2679-x]
  30. El-Gendy MMAA, Abdel-Moniem SM, Ammar NS et al (2023a) Multimetal bioremediation from aqueous solution using dead biomass of Mucor sp. NRCC6 derived from detergent manufacturing effluent. J Appl Genet 64:569���590. https://doi.org/10.1007/s13353-023-00765-9 [DOI: 10.1007/s13353-023-00765-9]
  31. El-Gendy MMAA, Abdel-Moniem SM, Ammar NS et al (2023b) Bioremoval of heavy metals from aqueous solution using dead biomass of indigenous fungi derived from fertilizer industry effluents: isotherm models evaluation and batch optimization. Biometals 36:1307���1329. https://doi.org/10.1007/s10534-023-00520-x [DOI: 10.1007/s10534-023-00520-x]
  32. Fazeka��ov�� D, Fazeka�� J (2020) Soil quality and heavy metal pollution assessment of iron ore mines in Nizna Slana (Slovakia). Sustainability 12:2549. https://doi.org/10.3390/su12062549 [DOI: 10.3390/su12062549]
  33. Greeff-Laubscher MR, Beukes I, Marais GJ, Karin J (2020) Mycotoxin production by three different toxigenic fungi genera on formulated abalone feed and the effect of an aquatic environment on fumonisins. Mycology 11(2):105���117 [DOI: 10.1080/21501203.2019.1604575]
  34. Hajihashemi S, Mbarki S, Skalicky M, Noedoost F, Raeisi M, Brestic M (2020) Effect of wastewater irrigation on photosynthesis, growth, and anatomical features of two wheat cultivars (Triticum aestivum L.). Water 12(2):607. https://doi.org/10.3390/w12020607 [DOI: 10.3390/w12020607]
  35. Ibrahim MIA, Mohamed LA, Mahmoud MG, Shaban KS, Fahmy MA, Ebeid MH (2019) Potential ecological hazards assessment and prediction of sediment heavy metals pollution along the Gulf of Suez, Egypt. Egypt J Aquat Res 45:329���335. https://doi.org/10.1016/j.ejar.2019.12.003 [DOI: 10.1016/j.ejar.2019.12.003]
  36. Knechtel RJ (1978) A more economical method for the determination of chemical oxygen demand. J Water Pollut Control Feder 116:25���29
  37. Kumar R, Kaur A (2018) Oil spill removal by mycoremediation. In: Kumar V, Kumar M, Prasad R (eds) Microbial action on hydrocarbons. Springer, Singapore. https://doi.org/10.1007/978-981-13-1840-5_20 [DOI: 10.1007/978-981-13-1840-5_20]
  38. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547���1549. https://doi.org/10.1093/molbev/msy096 [DOI: 10.1093/molbev/msy096]
  39. Kumar V, Sharma A, Kaur P, Preet GSS, Shreeya AB, Bhardwaj R, Kumar AT, Cerda A (2019) Pollution assessment of heavy metals in soils of India and ecological risk assessment: a state-of-the-art. Chemosphere 216:449���462. https://doi.org/10.1016/j.chemosphere.2018.10.066 [DOI: 10.1016/j.chemosphere.2018.10.066]
  40. Legorreta-Casta��eda J, Lucho-Constantino CA, Beltr��n-Hern��ndez RI, Coronel-Olivares C, V��zquez-Rodr��guez GA (2020) Biosorption of water pollutants by fungal pellets Adriana. Water 12:1155. https://doi.org/10.3390/w12041155 [DOI: 10.3390/w12041155]
  41. Mamitha KS, Grasian I, Albert HS (2013) Isolation and identification of hydrocarbon degrading bacteria from Ennore creek. Bioinformation 9(3):150���157 [DOI: 10.6026/97320630009150]
  42. Moretti A, Susca A (2017) Mycotoxigenic fungi: Methods and protocols, methods in molecular biology, vol 1542. Springer, New York. https://doi.org/10.1007/978-1-4939-6707-0_3 [DOI: 10.1007/978-1-4939-6707-0_3]
  43. Oyewole OA, Zobeashia SSLT, Oladoja EO et al (2019) Biosorption of heavy metal polluted soil using bacteria and fungi isolated from soil. SN Appl Sci 1:857. https://doi.org/10.1007/s42452-019-0879-4 [DOI: 10.1007/s42452-019-0879-4]
  44. Reeslev M, Kjoller A (1995) Comparison of biomass dry weights and radial growth rates of fungal colonies on media solidified with different gelling compounds. Appl Environ Microbiol 61(12):4236���4239. https://doi.org/10.1128/AEM.61.12.4236-4239.1995 [DOI: 10.1128/AEM.61.12.4236-4239.1995]
  45. Robert AS, J��nos V, Christian FJ (2011) Taxonomic studies on the genus Aspergillus- DTU orbit. CBS-KNAW Fungal Biodiversity Centre, Utrecht
  46. Sierra J, Mart�� E, Montserrat G, Cruanas R, Garau MA (2001) Characterisation and evolution of a soil affected by olive oil mill wastewater disposal. Sci Total Environ 279(1-3):207���214
  47. Silva LJG, Pereira AMPT, Pena A, Lino CM (2021) Citrinin in foods and supplements: a review of occurrence and analytical methodologies. Foods 10:14. https://doi.org/10.3390/foods10010014 [DOI: 10.3390/foods10010014]
  48. Solomon L, Tomii VP, Dick AA (2019) Importance of fungi in the petroleum, agro-allied, agriculture and pharmaceutical industries. N Y Sci J 12(5):8���15. https://doi.org/10.7537/marsnys120519.02 [DOI: 10.7537/marsnys120519.02]
  49. United Nations Educational, Scientific and Cultural Organization (UNESCO) (2017) A guide for ensuring inclusion and equity in education, Fontenoy 75352 Paris 07 SP, France. https://doi.org/10.54675/MHHZ2237
  50. Varjani S, Joshi R, Srivastava VK et al (2020) Treatment of wastewater from petroleum industry: current practices and perspectives. Environ Sci Pollut Res 27:27172���27180. https://doi.org/10.1007/s11356-019-04725-x [DOI: 10.1007/s11356-019-04725-x]
  51. Vieira FCS, Nahas E (2005) Comparison of microbial numbers in soils by using various culture media and temperatures. Microbiol Res 160(2):197���202 [DOI: 10.1016/j.micres.2005.01.004]
  52. Watanabe T (2002) Pictorial atlas of soil and seed fungi; morphologies of cultured fungi and key to species, 2nd edn. CRC Press, Boca Raton [DOI: 10.1201/9781420040821]
  53. Wei X, Zhang S, Sun Y, Brenner SA (2018) Petrochemical wastewater and produced water. Water Environ Res 90(10):1634���1647. https://doi.org/10.2175/106143018X15289915807344 [DOI: 10.2175/106143018X15289915807344]
  54. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315���322
  55. Wuana RA, Okieimen FE (2011) Heavy metals in polluted soils: a review of sources, chemistry, risks and best available strategies for remediation, Review Article. International Scholarly Research Notices, Article ID 402647.  https://doi.org/10.5402/2011/402647
  56. Xu R, Obbard JP (2003) Effect of nutrient amendments on indigenous hydrocarbon biodegradation in oil-polluted beach sediments. J Environ Qual 32(4):1234���1243. https://doi.org/10.2134/jeq2003.1234 [DOI: 10.2134/jeq2003.1234]
  57. Zhang C, Wu D, Ren H (2020a) Bioremediation of oil polluted soil using agricultural wastes via microbialconsortium. Sci Rep 10:9188. https://doi.org/10.1038/s41598-020-66169-5 [DOI: 10.1038/s41598-020-66169-5]
  58. Zhang D, Yin C, Abbas N et al (2020b) Multiple heavy metal tolerance and removal by an earthworm gut fungus Trichoderma brevicompactum QYCD-6. Sci Rep 10:6940. https://doi.org/10.1038/s41598-020-63813-y [DOI: 10.1038/s41598-020-63813-y]

Grants

  1. RSP2024R364/Deanship of Scientific Research, King Saud University

MeSH Term

Biodegradation, Environmental
Wastewater
Petroleum
Soil Pollutants
Soil Microbiology
Aspergillus
Penicillium
Saudi Arabia
Petroleum Pollution
Fungi
Metals
Soil
Hydrocarbons

Chemicals

Wastewater
Petroleum
Soil Pollutants
Metals
Soil
Hydrocarbons
Journal Article

Word Cloud

Created with Highcharts 10.0.0wastewaterpetroleumhydrocarbonsFA-KSU5soilfungalisolatesAspergillustubingensisnigerremovalsamplesmetalsaromaticgroupsFU-KSU69pollutedstrain98reductiontreatedsoilshumancelllinesbiomassFA-KSU69contaminatedvariousoilanalyzedtotalFeCrZnCuCdbioremediationefficiencyranging90achievedCoBaBVNiPbHg9315%TPHsdecreasePAHsexhibitedfollowedsignificantcytotoxicitynormaleffluentsdead��L/mLSEMIRanalysisnon-toxigenicstrainsenvironmentsHeavyfungiBioremediationSoilpetroleum-relatedindustriescollectedlocationsSaudiArabiacountryknownvastreservesphysicochemicalpropertiesincludingpresencecompounds264categorizedeight194fourPenicillium70potentialgrowderivativesinvestigatedTwoutilizedtworemediationexperiments-onetargetingfocusingdemonstratedcompleteMnsites8058%Additionally100%179602%180 mintreatment21 daysincubation48%8811%9731%polycyclichighestratesSe37%9490%9513%enzymaticactivityincreased154-357-foldcomparedAlthoughmixturehighfollowingmycoremediationshowedtoxicityconcentrations500ICvalues���������1000revealedmorphologicalbiochemicalalterationsexposedstudysuccessfullyintroducesenvironmentallyfriendlyplaycrucialroleservelow-costeffectiveadsorbentsbio-remediatingoil-contaminatedprimarypollutantseithercompletelyremovedreducedpermissiblelevelsaccordinginternationalguidelinesusingConsequentlyassociatedgloballyindustryrenderedbiologicallysafeparticularlyhumansevidencedabsencetypesoil-pollutedindigenousCellFungiPetroleumPolluted

Similar Articles

Cited By