Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-13T00:41:57.609Z Has data issue: false hasContentIssue false

Montmorillonite mitigates the toxic effect of heavy oil on hydrocarbon-degrading bacterial growth: implications for marine oil spill bioremediation

Published online by Cambridge University Press:  09 July 2018

S. K. Chaerun*
Affiliation:
Laboratory of Environmental Biogeosciences and Mining Bioengineering, Division of Genetics and Molecular Biotechnology, School of Life Sciences and Technology, Institut Teknologi Bandung, Ganesha 10, Bandung 40132, West Java, Indonesia Center for Life Sciences, Institut Teknologi Bandung, Indonesia
K. Tazaki
Affiliation:
University Professor Emerita, Kanazawa University, Kakuma, Kanazawa, Ishikawa 920-1192, Japan
M. Okuno
Affiliation:
Graduate School of Natural Science and Technology, Kanazawa University, Kakuma, Kanazawa, Ishikawa 920-1192, Japan
*

Abstract

The ability of montmorillonite to mitigate the toxic effect of heavy oil from the Nakhodka oil spill, by growth of hydrocarbon-degrading bacteria and enable bioremediation was studied. Montmorillonite enhanced the bacterial growth significantly (P < 0.05) in the main treatment containing heavy oil+bacteria+montmorillonite (OBM), because the specific growth rate (μ) was greater than that in the biotic control treatment containing heavy oil+bacteria (OB). Significant amounts of Si and Al (major constituents of montmorillonite) were not released in the aqueous phase over the ∽24-day experiment (P > 0.05). Transmission electron microscopic observation showed that the hydrocarbon-degrading bacterial cells were covered and encrusted with montmorillonite particles. Scanning transmission electron microscopy coupled with energy dispersive X-ray spectroscopy (STEM-EDS) also showed that the surrounding of the bacterial cells was frequently rich in Si but not in Al. Fourier transform infrared (FTIR) spectroscopy indicated that the heavy oil-bacterial cell-montmorillonite particle complex retained the composition of both water and heavy oil. X-ray powder diffractrometery (XRD) analysis revealed that heavy oil and heavy oil-bacteria did not change the basal spacing of montmorillonite over a period of 24 days. The enhancement of hydrocarbon-degrading bacterial growth is attributed to montmorillonite likely serving as both bacterial growth-supporting carrier and protective outer layer against high concentrations of heavy oil that inhibit growth. These results shed light on the interactions in oil-bacteria-clay complexes and could potentially be used in marine oil spill bioremediation.

Type
Research Article
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abed, R.M.M., Safi, N.M.D., Koster, J., de Beer, D., El-Nahhal, Y., Rullkotter, J. & Garcia-Pichel, F. (2002) Microbial diversity of a heavily polluted microbial mat and its community changes following degradation of petroleum compounds. Applied and Environmental Microbiology, 68, 1674–1683.CrossRefGoogle ScholarPubMed
Arun, A. & Eyini, M. (2011) Comparative studies on lignin and polycyclic aromatic hydrocarbons degradation by basidiomycetes fungi. Bioresource Technology, 102, 8063–8070.CrossRefGoogle ScholarPubMed
Boopathy, R. (2000) Factors limiting bioremediation technologies. Bioresource Technology, 74, 63–67.CrossRefGoogle Scholar
Chaerun, S. K. & Tazaki, K. (2005) How kaolinite plays an essential role in remediating oil-polluted seawater. Clay Minerals, 40, 481–491.CrossRefGoogle Scholar
Chaerun, S.K., Tazaki, K., Asada, R. & Kogure, K. (2004) Bioremediation of coastal areas 5 years after the Nakhodka oil spill in the Sea of Japan: isolation and characterization of hydrocarbon-degrading bacteria. Environment International, 30, 911–922.CrossRefGoogle ScholarPubMed
Chaerun, S.K., Tazaki, K., Asada, R. & Kogure, K. (2005) Interaction between clay minerals and hydrocarbonutilizing indigenous microorganisms in high concentration of heavy oil: Implications for bioremediation. Clay Minerals, 40, 105–114.Google Scholar
Chenu, C. (1993) Clay- or sand-polysaccharide associations as models for the interface between microorganisms and soil: water related properties and microstructure. Geoderma, 56, 143–156.CrossRefGoogle Scholar
Chenu, C. & Jaunet, A. M. (1992) Cryoscanning electron microscopy of microbial extracellular polysaccharides and their association with minerals. Scanning, 14, 360–364.CrossRefGoogle Scholar
Chenu, C. & Plante, A. F. (2006) Clay-sized organomineral complexes in a cultivation chronosequence: revisiting the concept of the primary organo-mineral complex. European Journal of Soil Science, 57, 596–607.CrossRefGoogle Scholar
Chenu, C. & Tessier, D. (1995) Low temperature scanning electron microscopy of clay and organic constituents and their relevance to soil microstructures. Scanning Microscopy, 9, 989–1010.Google Scholar
de Lorenzo, V. (2006) Blueprint of an oil-eating bacterium. Nature Biotechnology, 24, 952–953.CrossRefGoogle ScholarPubMed
Dong, H., Kostka, J. E. & Kim, J. (2003) Microscopic evidence for microbial dissolution of smectite. Clays and Clay Minerals, 51, 502–512.CrossRefGoogle Scholar
Flemming, H.-C. & Wingender, J. (2010) The biofilm matrix. Nature Reviews, Microbiology, 8, 623–633.Google Scholar
Ganidi, N., Tyrrel, S. & Cartmell, E. (2009) Anaerobic digestion foaming causes – a review. Bioresource Technology, 100, 5546–5554.CrossRefGoogle ScholarPubMed
Gates, W.P., Jaunet, A.-M., Tessier, D., Cole, M.A., Wilkinson, H. T. & Stucki, J. W. (1998) Swelling and texture of iron-bearing smectites reduced by bacteria. Clays and Clay Minerals, 46, 487–497.CrossRefGoogle Scholar
Hallett, P. D. & Young, I. M. (1999) Changes to water repellence of soil aggregates caused by substrateinduced microbial activity. European Journal of Soil Science, 50, 35–40.CrossRefGoogle Scholar
Harayama, S., Kishira, H., Kasai, Y. & Shutsubo, K. (1999) Petroleum biodegradation in marine environments. Journal of Molecular Microbiology and Biotechnology, 1, 63–70.Google ScholarPubMed
Head, I. M. & Swannell, R. P. (1999) Bioremediation of petroleum hydrocarbon contaminants in marine habitats. Current Opinion in Biotechnology, 10, 234–239.CrossRefGoogle ScholarPubMed
Hundal, L.S., Thompson, M.L., Laird, D. A. & Carmo, A. M. (2001) Sorption of phenanthrene by reference smectites. Environmental Science & Technology, 35, 3456–3461.CrossRefGoogle ScholarPubMed
Iwabuchi, N., Sunairi, M., Urai, M., Itoh, C., Anzai, H., Nakajima, M. & Harayama, S. (2002) Extracellular polysaccharides of Rhodococcus rhodochrous S-2 stimulate the degradation of aromatic components in crude oil by indigenous marine bacteria. Applied and Environmental Microbiology, 68, 2337–2343.CrossRefGoogle ScholarPubMed
Juhasz, A. L. & Naidu, R. (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]- pyrene. International Biodeterioration & Biodegradation, 45, 57–88.CrossRefGoogle Scholar
Kanaly, R. A. & Harayama, S. (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. Journal of Bacteriology, 182, 2059–2067.CrossRefGoogle ScholarPubMed
Maki, H., Utsumi, M., Koshikawa, H., Hiwatari, T., Kohata, K., Uchiyama, H., Suzuki, M., Noguchi, T., Yamasaki, T., Furuki, M. & Watanabe, M. (2003) Intrinsic biodegradation of heavy oil from Nakhodka and the effect of exogenous fertilization at a coastal area of the sea of Japan. Water, Air, and Soil Pollution, 145, 123–138.CrossRefGoogle Scholar
Martinez-Checa, F., Toledo, F.L., El Mabrouki, K., Quesada, E. & Calvo, C. (2007) Characteristics of bioemulsifier V2-7 synthesized in culture media added of htdrocarbons: Chemical composition, emulsifying activity and rheological properties. Bioresource Technology, 98, 3130–3135.CrossRefGoogle ScholarPubMed
Megharaj, M., Singleton, I., McClure, N. C. & Naidu, R. (2000) Influence of petroleum hydrocarbon contamination on microalgae and microbial activities in a long-term contaminated soil. Archives of Environmental Contamination and Toxicology, 38, 439–445.CrossRefGoogle Scholar
Mulligan, C. N. (2005) Environmental applications for biosurfactants. Environmental Pollution, 133, 183–198.CrossRefGoogle ScholarPubMed
Nikolopoulou, M. & Kalogerakis, N. (2008) Enhanced bioremediation of crude oil utilizing lipophilic fertilizers combined with biosurfactants and molasses. Marine Pollution Bulletin, 56, 1855–1861.CrossRefGoogle ScholarPubMed
Prince, R. C. (1993) Petroleum spill bioremediation in marine environments. Critical Reviews in Microbiology, 19, 217–242.CrossRefGoogle ScholarPubMed
Reddy, M., Naresh, S., Leela, T., Prashanthi, M., Madhusudhan, N.C., Dhanasri, G. & Devi, P. (2010) Biodegradation of phenanthrene with biosurfactant production by a new strain of Brevibacillus sp. Bioresource Technology, 101, 7980–7983.CrossRefGoogle ScholarPubMed
Ron, E. Z. & Rosenberg, E. (2001) Natural roles of biosurfactants. Environmental Microbiology, 3, 229–236.CrossRefGoogle ScholarPubMed
Ron, E. Z. & Rosenberg, E. (2002) Biosurfactants and oil bioremediation. Current Opinion in Biotechnology, 13, 249–252.CrossRefGoogle ScholarPubMed
Stotzky, G. (1986) Influence of soil mineral colloids on metabolic processes, growth, adhesion, and ecology of microbes and viruses. Pp. 305–428 in: Interaction of Soil Minerals with Natural Organics and Microbes (Huang, P.M. & Schnitzer, M., editors). Soil Science Society of America, Madison, Wisconsin.Google Scholar
Swannell, R.P., Lee, K. & McDonagh, M. (1996) Field evaluations of marine oil spill bioremediation. Microbiological Reviews, 60, 342–365.CrossRefGoogle ScholarPubMed
Tazaki, K., editor (2003) Heavy oil spilled from Russian tanker “Nakhodka” in 1997: towards eco-responsibility, earth sense. Kanazawa University Press, 21st Century COE, Kanazawa University, Japan.Google Scholar
Zhang, Y. & Miller, R. M. (1994) Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Applied and Environmental Microbiology, 60, 2101–2106.CrossRefGoogle ScholarPubMed