Log in

Selective metal accumulation by metal-resistant bacteria growing on spent engine oil in single and ternary metal mixtures

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

Three metal-resistant bacteria species, identified as Pseudomonas alcaligenes B101, Pseudomonas fluorescens C101 and Stenotrophomonas maltophilia E103, isolated from spent engine oil-contaminated tropical soils utilised spent engine oil (SEO) as a source of nutrient for growth in the presence of Pb2+ (500 µg/ml), Cu2+ (400 µg/ml) and Zn2+ (400 µg/ml) with concomitant cellular accumulation of the metals in single and ternary mixtures. Degradation of SEO in the presence of the metals and their mixture within a 21 days experimental period ranged between 27.8 and 57.8% compared to 52.2% and 66.7% in metal free controls with extensive modification (up to 92.7%) of the aromatic fractions of the spent oil. Cellular accumulation of the metals during SEO degradation ranged between 0.13 and 30.76%, and 3.77% and 33.43%, respectively, in growth media supplemented with single metal ions and their mixtures. Stenotrophomonas maltophilia E103 showed the best potential for metal uptake, accumulating the highest concentration of Pb2+ (29.0%) and Zn2+ (30.8%) in systems supplemented with single metals, while P. alcaligenes B101 and P. fluorescens C101 showed preference for the accumulation of Pb2+ (15.1%) and Cu2+ (23.8%), respectively. Although metal uptake decreased significantly in ternary metal systems, strains B101 and E103 maintained their preferences for Pb2+ in the ternary systems. The ability of these bacteria to metabolise spent engine oil with concurrent intracellular metal accumulation in the presence of high concentrations of Pb2+, Cu2+ and Zn2+ and their mixtures highlighted their potentials for use in the remediation of sites exposed to hydrocarbon-metal co-contamination.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ali N, Dashti N, Al-Mailem D, Eliyas M, Radwan D (2012) Indigenous soil bacteria with the combined potential for hydrocarbon consumption and heavy metal resistance. Environ Sci Pollut Res 19:812–820. https://doi.org/10.1007/s11356-011-0624-z-

    Article  CAS  Google Scholar 

  • Alisi C, Musella R, Tasso F, Ubaldi C, Manzo S, Cremisini C, Sprocati AR (2009) Bioremediation of diesel oil in a co-contaminated soil bioaugmentation with a microbial formula tailored with native strains selected for heavy metal resistance. Sci Total Environ 407:3024–3032

    Article  CAS  Google Scholar 

  • American Society for Testing and Materials (ASTM) (1995) Annual book of ASTM standards, designation D4972-95a: standard test method for pH of soils. ASTM, West Conshohocken

    Google Scholar 

  • APHA (1998) Standard methods for the examination of water and waste water 20th American Public Health Association, American Water Works Association, Water Environment Federation. APHA, Washington, DC

    Google Scholar 

  • Arjoon A, Olaniran OO, Balgobind A, Pillay B (2013) Enhanced 1,2 dichloroethane degradation in heavy metal co-contaminated wastewater undergoing biostimulation and bioaugmentation. Chemosphere 93:1826–1834

    Article  CAS  Google Scholar 

  • ATSDR (1997) Public health statements: used mineral based crankcase oil. ATSDR, Atlanta

    Google Scholar 

  • Benka-Coker MO, Ekundayo JA (1998) Effects of heavy metals on growth of species of Micrococcus and Pseudomonas in a crude oil/minerals salts medium. Bioresour Technol 66:241–245

    Article  CAS  Google Scholar 

  • Boullemant A, Lavoie M, Fortin C, Campbell PGC (2009) Uptake of hydrophobic metal complexes by three freshwater algae: unexpected influence of pH. Environ Sci Technol 43:3308–3314

    Article  CAS  Google Scholar 

  • Cao Y, Liu Z, Cheng G, **g X, Xu H (2010) Exploring single and multi-metal biosorption by immobilised spent Tricholoma lobayense using multi-step response surface methodology. Chem Eng J 164:183–195

    Article  CAS  Google Scholar 

  • Castillo-Zacarías CJ, Suárez-Herrera MA, Garza-González MT, Sánchez-González MN, López-Chuken UJ (2011) Biosorption of metals by phenol-resistant bacteria isolated from contaminated industrial effluents. Afr J Microbiol Res 5:2627–2631

    Article  Google Scholar 

  • Chen Z, Zhu L, Wilkinson KJ (2010) Validation of the biotic ligand model (BLM) in metal mixtures: bioaccumulation of lead and copper. Environ Sci Technol 44:3580–3586

    Article  CAS  Google Scholar 

  • Chen A, Zeng G, Chen G, Fan J, Zou Z, Li H, Hu X, Long F (2011) Simultaneous cadmium removal and 2,4-dichlorophenol degradation from aqueous solutions by Phanerochaete chrysosporium. Appl Microbiol Biotechnol 91:811–821

    Article  CAS  Google Scholar 

  • Chen S, Yin H, Ye J, Peng H, Zhang N, He B (2013) Effect of Copper (II) on biodegradation of Benzo[a]pyrene by Stenotrophomonas maltophilia. Chemosphere 90:1811–1820

    Article  CAS  Google Scholar 

  • Coimbra CD, Rufino RD, Luna JM, Sarubbo LA (2009) Studies of the cell surface properties of Candida species and relation to the production of biosurfactants for environmental applications. Curr Microbiol 58:245–251

    Article  CAS  Google Scholar 

  • Hanlon Jr. EA (2015) Soil pH and electrical conductivity: a county extension soil laboratory manual. University of Florida/Institute of Food and Agricultural Sciences Extension Paper CIR1081. Available at http://edis.ifas.ufl.edu. Accessed 3 Sept 2014

  • Fagundes-Klen MR, Vaz LGL, Veit MT, Borba CE, Silva EA, Kroumov AD (2007) Biosorption of the copper and cadmium ions—a study through adsorption isotherms analysis. Bioautomation 7:23–33

    Google Scholar 

  • Flouty R, Estephane G (2012) Bioaccumulation and biosorption of copper and lead by a unicellular algae Chlamydomonas reinhardtii in single and binary metal systems: a comparative study. J Environ Manag 111:106–114

    Article  CAS  Google Scholar 

  • Franҫois F, Lombard C, Guigner JM, Soreau P, Brian-Jaisson F, Martino G, Vandervennet M, Garcia D, Molinier AL, Peducci J, Zirah S, Rebuffat S (2012) Isolation and characterization of environmental bacteria capable of extracellular biosorption of mercury. Appl Environ Microbiol 78:1097–1106

    Article  CAS  Google Scholar 

  • Gauthier PT, Norwood WP, Prepas EE, Pyle GG (2014) Metal-PAH mixtures in the aquatic environment: a review of co-toxic mechanisms leading to more-than-additive outcomes. Aquat Toxicol 154:253–269

    Article  CAS  Google Scholar 

  • Ge W, Zamri D, Mineyama H, Valix M (2011) Bioaccumulation of heavy metals on adapted Aspergillus foetidus. Adsorpt J Int Adsorpt Soc 17:901–910

    Article  CAS  Google Scholar 

  • Kumar A, Kumar S, Kumar S (2005) Biodegradation kinetics of phenol and catechol using Pseudomonas putida MTCC 1194. Biochem Eng J 22:151–159

    Article  CAS  Google Scholar 

  • Lavoie M, Le Faucheur S, Boullemant A, Fortin C, Campbell PGC (2012) The influence of pH on algal cell membrane permeability and its implication for the uptake of lipophilic metal complexes. J Phycol 48:293–302

    Article  CAS  Google Scholar 

  • Lin YB, Wang XY, Wang BP, Mohamad O, Wei GH (2012) Bioaccumulation characterization of zinc and cadmium by Streptomyces zinciresistens, a novel actinomycete. Ecotoxicol Environ Saf 77:7–17

    Article  CAS  Google Scholar 

  • Lu WB, Kao WC, Shi JJ, Chang JS (2008) Exploring multi-metal biosorption by indigenous metal-hyperresistant Enterobacter sp. 1 using experimental design methodologies. J Hazard Mater 153:372–381

    Article  CAS  Google Scholar 

  • Lu M, Zhang ZZ, Wu XJ, Xu YX, Su XL, Zhang M, Wang JX (2013) Biodegradation of decabromodiphenyl ether (BDE-209) by a metal resistant strain, Bacillus cereus JP12. Bioresour Technol 149:8–15

    Article  CAS  Google Scholar 

  • Mahamadi C, Nharingo T (2010) Competitive adsorption of Pb2+, Cd2+ and Zn2+ ions onto Eichhornia crassipes in binary and ternary systems. Bioresour Technol 101:859–864

    Article  CAS  Google Scholar 

  • Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278

    Article  CAS  Google Scholar 

  • Mohapatra H, Gupta R (2005) Concurrent sorption of Zn(II), Cu(II) and Co(II) by Oscillatoria angustissima as a function of pH in binary and ternary metal solutions. Bioresour Technol 96:1387–1398

    Article  CAS  Google Scholar 

  • Nakajima A, Sakaguchi T (1986) Selective accumulation of heavy metals by microorganisms. Appl Microbiol Biotechnol 24:59–64

    CAS  Google Scholar 

  • National Environmental Standards and Regulations Enforcement Agency (NESREA) (2011) National environmental (surface and ground-water quality control) regulations (S.I. 22 of 2011)

  • Norwood WP, Borgmann U, Dixon DG, Wallace A (2003) Effects of metal mixtures on aquatic biota: a review of observations and methods. Hum Ecol Risk Assess 9:795–811

    Article  CAS  Google Scholar 

  • Olaniran OO, Balgobind A, Pillay B (2011) Quantitative assessment of the toxic effects of heavy metals on 1,2-dichloroethane biodegradation in co-contaminated soil under aerobic conditions. Chemosphere 85:839–845

    Article  CAS  Google Scholar 

  • Onojake MC, Osuji LC (2012) Assessment of the physicochemical properties of hydrocarbon contaminated soil. Arch Appl Sci Res 4(4):48–58

    CAS  Google Scholar 

  • Oriomah C, Adelowo OO, Adekanmbi AO (2015) Bacteria from spent engine-oil-contaminated soils possess dual tolerance to hydrocarbon and heavy metals, and degrade spent oil in the presence of copper, lead, zinc and combinations thereof. Ann Microbiol 65:207–215

    Article  CAS  Google Scholar 

  • Oyetibo GO, Ilori MO, Obayori OS, Amund OO (2013) Biodegradation of petroleum hydrocarbons in the presence of nickel and cobalt. J Basic Microbiol 53:917–927

    Article  CAS  Google Scholar 

  • Oyetibo GO, Ilori MO, Obayori OS, Amund OO (2015) Metal biouptake by actively growing cells of metal-tolerant bacteria strains. Environ Monit Assess 187:525. https://doi.org/10.1007/s10661-015-4731-z

    Article  CAS  Google Scholar 

  • Pakshirajan K, Swaminathan T (2009) Biosorption of lead, copper and cadmium by Phanerochaete chrysosporium in ternary metal mixtures: statistical analysis of individual and interaction effects. Appl Biochem Biotechnol 158:457–489

    Article  CAS  Google Scholar 

  • Pérez-Marín AB, Ballester A, González F, Blázquez ML, Muñoz JA, Sáez J, Zapata M (2008) Study of cadmium, zinc and lead biosorption by orange wastes using the subsequent addition method. Bioresour Technol 99:8101–8106

    Article  CAS  Google Scholar 

  • Ruangosomboon S, Wongrat S, Choochote S, Guanmanee M, Saparnklang A (2013) Effects of low pH and Pb2+ stress on living cyanobaterium, Phormidium angustissimum West and G. S. West: a test of its feasibility as living biosorbent. J Appl Phycol 25:905–911

    Article  CAS  Google Scholar 

  • Saimmai A, Kaewrueng J, Maneerat S (2012) Used lubricating oil degradation and biosurfactant production by SC-9 consortia obtained from oil contaminated soil. Ann Microbiol 62:1757–1767

    Article  CAS  Google Scholar 

  • Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093–1101

    Article  CAS  Google Scholar 

  • Selenska-Pobell S, Panak P, Miteva V, Boudakov I, Bernhard G, Nitsche H (1999) Selective accumulation of heavy metals by three indigenous Bacillus strains, B. cereus, B. megaterium and B. sphaericus from drain waters of a uranium waste pile. FEMS Microbiol Ecol 29:59–67

    Article  CAS  Google Scholar 

  • Sneath PHA (1996) Bergey’s manual of determinative bacteriology. William and Wilkins, Baltimore

    Google Scholar 

  • Tao Y, Xue B, Yang Z, Yao S, Li S (2015) Effects of metals on the uptake of polycyclic aromatic hydrocarbon by the cyanobacterium Microcystis aeruginosa. Chemosphere 119:719–726

    Article  CAS  Google Scholar 

  • Tsezos M, Remoudaki E, Anglelatou V (1996) A study of the effects of competing ions on the biosorption of metals. Int Biodeterior Biodegrad 38:19–29

    Article  CAS  Google Scholar 

  • USEPA (1990) Acid digestion of sediments, sludge and soils. USEPA SW-S846; Ch 3.2 Method 3050 A; US Environmental Protection Agency. Government Print Office, Washington, DC

    Google Scholar 

  • USEPA (1996) Recycling used oil: what can you do? Cooperation extension services ENRI 317:1–2

    Google Scholar 

  • USEPA (2011) Priority pollutants. United States Environmental Protection Agency. http://water.epa.gov/scitech/methods/cwa/pollutants.cfm. Accessed 27 Aug 2015

  • Villalobos M, Avila-Forcada AP, Gutierrez-Ruiz ME (2008) An improved gravimetric method to determine total petroleum hydrocarbons in contaminated soils. Water Air Soil Pollut 194:151–161

    Article  CAS  Google Scholar 

  • Worms IAM, Wilkinson KJ (2007) Ni uptake by green algae. 2. Validation of equilibrium models for competition effects. Environ Sci Technol 41:4264–4270

    Article  CAS  Google Scholar 

  • Xu N, Bao M, Sun P, Li Y (2013) Study on bioadsorption and biodegradation of petroleum hydrocarbons by a microbial consortium. Bioresour Technol 149:22–30

    Article  CAS  Google Scholar 

  • Yan C, Li G, Xue P, Wei Q, Li Q (2010) Competitive effect of Cu(II) and Zn(II) on the biosorption of lead (II) by Myriophyllum spicatum. J Hazard Mater 179:721–728

    Article  CAS  Google Scholar 

  • Yin H, He BY, Peng H, Ye JS, Yang F, Zhang N (2008) Removal of Cr(VI) and Ni (II) from aqueous solution by fused yeast: study of cations release and biosorption mechanism. J Hazard Mater 158:568–576

    Article  CAS  Google Scholar 

  • Zajic JE, Supplisson B (1972) Emulsification and Degradation of ‘Bunker C’ Fuel Oil by Microorganisms. Biotechnol Bioeng 14:331–343

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to the owners of the ARGs who allowed sample collection from their workshops and to Mr Femi Babalola of the Department of Chemistry and the Basel Convention Centre, the University of Ibadan who assisted in interpreting the GC-FID data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. O. Adelowo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Editorial responsibility: M. Abbaspour.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Fig S1

Metal resistance profiles of the isolated bacteria (XLSX 12 kb)

Fig S2

GC-FID chromatogram of residual SEO from (a) control; (b) P. alcaligenes B101; (c) P. fluorescens C101 and (d) S. maltophilia E103 after 21 days (DOCX 1106 kb)

Fig S3

Changes in pH with time for (a) P. alcaligenes B101 (b) P. fluorescens C101, (c) S. maltophilia E103 during growth on SEO (XLSX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ikhimiukor, O.O., Adelowo, O.O. Selective metal accumulation by metal-resistant bacteria growing on spent engine oil in single and ternary metal mixtures. Int. J. Environ. Sci. Technol. 16, 4945–4954 (2019). https://doi.org/10.1007/s13762-018-2137-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-018-2137-5

Keywords

Navigation