Characterization of biosurfactants produced by the oil-degrading bacterium Rhodococcus erythropolis S67 at low temperature

Luong, T. M.; Ponamoreva, O. N.; Nechaeva, I. A.; Petrikov, K. V.; Delegan, Ya. A.; Surin, A. K.; Linklater, D.; Filonov, A. E.

doi:10.1007/s11274-017-2401-8

Original Paper
Published: 04 January 2018

Characterization of biosurfactants produced by the oil-degrading bacterium Rhodococcus erythropolis S67 at low temperature

World Journal of Microbiology and Biotechnology volume 34, Article number: 20 (2018) Cite this article

799 Accesses
18 Citations
Metrics details

Abstract

Production of trehalolipid biosurfactants by Rhodococcus erythropolis S67 depending on the growth temperature was studied. R. erythropolis S67 produced glycolipid biosurfactants such as 2,3,4-succinoyl-octanoyl-decanoyl-2′-decanoyl trehalose and 2,3,4-succinoyl-dioctanoyl-2′-decanoyl trehalose during the growth in n-hexadecane medium at 26 and 10 °C, despite the different aggregate state of the hydrophobic substrate at low temperature. The surface tension of culture medium was found being reduced from 72 to 27 and 45 mN m⁻¹, respectively. Production of trehalolipid biosurfactants by R. erythropolis S67 at low temperature could be useful for the biodegradation of petroleum hydrocarbons at low temperatures by enhancing the bioremediation performance in cold regions.

Graphical abstract

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Abu-Ruwaida A, Banat I, Haditirto S, Salem A, Kadri M (1991) Isolation of biosurfactant-producing bacteria, product characterization, and evaluation. Acta Biotechnol 11:315–324. https://doi.org/10.1002/abio.370110405
CAS Article Google Scholar
Ausubel F, Brent R, Kingston R, Moore D, Seidman J, Struhl K (2003) Current protocols in molecular biology. Wiley, New York, pp 180–183
Google Scholar
Ciapina EM, Melo WC, Santa Anna LM, Santos AS, Freire DM, Pereira Junior N (2006) Biosurfactant production by Rhodococcus erythropolis grown on glycerol as sole carbon source. Appl Biochem Biotechnol 129–132:880–886. https://doi.org/10.1007/978-1-59745-268-7_72
Article Google Scholar
Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53:224–229
CAS Google Scholar
Dang NP, Landfald B, Willassen NP (2016) Biological surface-active compounds from marine bacteria. Environ Technol 37:1151–1158. https://doi.org/10.1080/09593330.2015.1103784
CAS Article Google Scholar
De Carvalho CC (2012) Adaptation of Rhodococcus erythropolis cells for growth and bioremediation under extreme conditions. Res Microbiol 163:125–135. https://doi.org/10.1016/j.resmic.2011.11.003
Article Google Scholar
De Carvalho CC, Da Fonseca MM (2005) Degradation of hydrocarbons and alcohols at different temperatures and salinities by Rhodococcus erythropolis DCL14. FEMS Microbiol Ecol 51:389–399. https://doi.org/10.1016/j.femsec.2004.09.010
Article Google Scholar
Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64
CAS Google Scholar
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determnation of sugers and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
CAS Article Google Scholar
Evans C, Herbert D, Tempest D (1970) The continuous cultivation of microorganisms. In: Norris JR, Ribbons DW (eds) Methods of microbiology. 2. Construction of a chemostat. Academic Press, London, pp 277–327
Google Scholar
Franzetti A, Gandolfi I, Bestetti G, Smyth T, Banat I (2010) Production and applications trehalose lipid biosurfactants. Eur J Lipid Sci Technol 120:617–627. https://doi.org/10.1002/ejlt.200900162
Article Google Scholar
Ivshina IB, Kuyukina MS, Philp JC, Christofi N (1998) Oil desorption from mineral and organic materials using biosurfactant complexes produced by Rhodococcus species. World J Microbiol Biotechnol 14:711–717. https://doi.org/10.1023/A:1008885309221
CAS Article Google Scholar
Li C, Zhou ZX, Jia XQ, Chen Y, Liu J, Wen JP (2013) Biodegradation of crude oil by a newly isolated strain Rhodococcus sp. JZX-01. Appl Biochem Biotechnol 171:1715–1725. https://doi.org/10.1007/s12010-013-0451-4
CAS Article Google Scholar
Luong TM, Nechaeva IA, Petrikov KV, Puntus IF, Ponamoreva ON (2016) Oil-degrading microorganisms of genus Rhodococcus: potential producers of biosurfactants (article in Russian). Izvestiya Vuzov. Prikladnaya Khimiya i Biotekhnologiya 1:50–60
Google Scholar
Malavenda R, Rizzo C, Michaud L (2015) Biosurfactant production by Arctic and Antarctic bacteria growing on hydrocarbons. Polar Biol 38:1565–1574. https://doi.org/10.1007/s00300-015-1717-9
Article Google Scholar
Margesin R, Moertelmaier C, Mair J (2013) Low-temperature biodegradation of petroleum hydrocarbons (n-alkanes, phenol, anthracene, pyrene) by four actinobacterial strains. Int Biodeterior Biodegrad 84:185–191. https://doi.org/10.1016/j.ibiod.2012.05.004
CAS Article Google Scholar
Marques A, Pinazo A, Farfan M, Aranda F, Teruel J, Ortiz A, Manresa A, Espuny M (2009) The physicochemical properties and chemical composition of trehalose lipids produced by Rhodococcus erythropolis 51T7. Chem Phys Lipids 158:110–117. https://doi.org/10.1016/j.chemphyslip.2009.01.001
CAS Article Google Scholar
McDonald R, Knox OG (2014) Cold region bioremediation of hydrocarbon contaminated soils: do we know enough? Environ Sci Technol 48:9980–9981. https://doi.org/10.1021/es5036738
CAS Article Google Scholar
Mutalik SR, Vaidya BK, Joshi RM, Desai KM, Nene SN (2008) Use of response surface optimization for the production of biosurfactant from Rhodococcus spp. MTCC 2574. Bioresour Technol 99:7875–7880. https://doi.org/10.1016/j.biortech.2008.02.027
CAS Article Google Scholar
Niescher S, Lang S, Kaschabek S, Schlomann M (2006) Identification and structural characterization of novel trehalose dinocardiomycolates from n-alkane-grown Rhodococcus opacus 1CP. Appl Microbiol Biotechnol 70:605–611. https://doi.org/10.1007/s00253-005-0113-8
CAS Article Google Scholar
Paulino BN, Pessoa MG, Mano MC, Molina G, Neri-Numa IA, Pastore GM (2016) Current status in biotechnological production and applications of glycolipid biosurfactants. Appl Microbiol Biotechnol 100:10265–10293. https://doi.org/10.1007/s00253-016-7980-z
CAS Article Google Scholar
Peng F, Liu Z, Wang L, Shao Z (2007) An oil-degrading bacterium: Rhodococcus erythropolis strain 3C-9 and its biosurfactants. J Appl Microbiol 102: 1603–1611. https://doi.org/10.1111/j.1365-2672.2006.03267.x
CAS Article Google Scholar
Petrikov K, Delegan Y, Surin A, Ponamoreva O, Puntus I, Filonov A, Boronin A (2013) Glycolipids of Pseudomonas and Rhodococcus oil-degrading bacteria used in bioremediation preparations: formation and structure. Process Biochem 48:931–935. https://doi.org/10.1016/j.procbio.2013.04.008
CAS Article Google Scholar
Philp J, Kuyukina M, Ivshina I, Dunbar S, Christofi N, Lang S, Wray V (2002) Alkanotrophic Rhodococcus ruber as a biosurfactant producer. Appl Microbiol Biotechnol 59:318–324. https://doi.org/10.1007/s00253-002-1018-4
CAS Article Google Scholar
Pirog TP, Shevchuk TA, Voloshina IN, Karpenko EV (2004) Production of surfactants by Rhodococcus erythropolis strain EK-1, grown on hydrophilic and hydrophobic substrates. Appl Biochem Mirobiol 40:470–475
CAS Article Google Scholar
Pyrchenkova IA, Gafarov AB, Puntus IF, Filonov AE, Boronin AM (2006) Selection and characterization of active psychtrophic microbial oil-degrading microorganisms. Appl Biochem Mirobiol 42:263–269. https://doi.org/10.1134/s0003683806030070
CAS Article Google Scholar
Rapp P, Gabriel-Jurgens LH (2003) Degradation of alkanes and highly chlorinated benzenes, and production of biosurfactants, by a psychrophilic Rhodococcus sp. and genetic characterization of its chlorobenzene dioxygenase. Microbiology 149:2879–2890. https://doi.org/10.1099/mic.0.26188-0
CAS Article Google Scholar
Sadouk Z, Hacene H, Tazerouti A (2008) Biosurfactants production from low cost substrate and degradation of diesel oil by a Rhodococcus strain. Oil Gas Sci Technol Rev IFP Energ Nouvelles 63:747–753. https://doi.org/10.2516/ogst:2008037
CAS Article Google Scholar
Shavandi M, Mohebali G, Haddadi A, Shakarami H, Nuhi A (2011) Emulsification potential of a newly isolated biosurfactant-producing bacterium, Rhodococcus sp. strain TA6. Colloids Surf B 82:477–482. https://doi.org/10.1016/j.colsurfb.2010.10.005
CAS Article Google Scholar
Smyth TJP, Perfumo A, Marchant R, Banat IM (2010) Isolation and analysis of low molecular weight microbial glycolipids. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 3705–3724
Chapter Google Scholar
Tamura K, Stecher G, Peterson D, Filipski J, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
CAS Article Google Scholar
Tokumoto Y, Nomura N, Uchiyama H, Imura T, Morita T, Fukuoka T, Kitamoto D (2009) Structural characterization and surface-active properties of a succinoyl trehalose lipid produced by Rhodococcus sp. SD-74. J Oleo Sci 58:97–102. https://doi.org/10.5650/jos.58.97
CAS Article Google Scholar
Tuleva B, Christova N, Cohen R, Stoev G, Stoineva I (2008) Production and structural elucidation of trehalose tetraesters (biosurfactants) from a novel alkanothrophic Rhodococcus wratislaviensis strain. J Appl Microbiol 104: 1703–1710. https://doi.org/10.1111/j.1365-2672.2007.03680.x
CAS Article Google Scholar
Uchida Y, Tsuchiya R, Chino M, Hirano J, Tabuchi T (1989) Extracellular accumulation of mono- and di-succinoyl trehalose lipids by a strain of Rhodococcus erythropolis grown on n-alkanes. Agric Biol Chem 53:757–763. https://doi.org/10.1271/bbb1961.53.757
CAS Google Scholar
Van Stempvoort D, Biggar K (2008) Potential for bioremediation of petroleum hydrocarbons in groundwater under cold climate conditions: a review. Cold Reg Sci Technol 53:16–41. https://doi.org/10.1016/j.coldregions.2007.06.009
Article Google Scholar
White D, Hird L, Ali S (2013) Production and characterization of a trehalolipid biosurfactant produced by the novel marine bacterium Rhodococcus sp. strain PML026. J Appl Microbiol 115:744–755. https://doi.org/10.1111/jam.12287
CAS Article Google Scholar
Whyte LG, Zhou HJ, Bourbonnière E, Inniss L, Greer WE, Charles W (1998) Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Appl Environ Microbiol 64:2578–2584
CAS Google Scholar
Whyte LG, Slagman SJ, Pietrantonio F, Bourbonniere L, Koval SF, Lawrence JR, Inniss WE, Greer CW (1999) Physiological adaptations involved in alkane assimilation at a low temperature by Rhodococcus sp. strain Q15. Appl Environ Microbiol 65:2961–2968
CAS Google Scholar
Yamamoto S, Harayama S (1995) PCR amplification and direct sequencing of gyrB genes with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Appl Environ Microbiol 61:1104–1109
CAS Google Scholar
Zheng C, Shuguang L, Li Y, Lixin H, Qinghong W (2009) Study of the biosurfactant-producing profile in a newly isolated Rhodococcus ruber strain. Ann Microbiol 59:771–777. https://doi.org/10.1007/BF03179222
CAS Article Google Scholar

Download references

Acknowledgements

The results of the research project are published with the financial support of Tula State University within the framework of the scientific project No. 8709. The biodegradation work has been supported by RFBR Grant No. 16-34-00610.

Author information

Affiliations

Biotechnology Department, Tula State University, 92 Lenin Av., Tula, 300012, Russian Federation
T. M. Luong, O. N. Ponamoreva & I. A. Nechaeva
G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, 5 Nauki Av., Pushchino, Moscow Region, 142290, Russian Federation
K. V. Petrikov, Ya. A. Delegan & A. E. Filonov
Institute of Protein Research, Russian Academy of Sciences, 4 Nauki Av., Pushchino, Moscow Region, 142290, Russian Federation
A. K. Surin
Swinburne University of Technology, PO Box 218, Hawthorn, VIC, 3122, Australia
D. Linklater
Pushchino State Natural Science Institute, 3 Nauki Av., Pushchino, Moscow Region, 142290, Russian Federation
Ya. A. Delegan

Authors

T. M. Luong
View author publications
You can also search for this author in PubMed Google Scholar
O. N. Ponamoreva
View author publications
You can also search for this author in PubMed Google Scholar
I. A. Nechaeva
View author publications
You can also search for this author in PubMed Google Scholar
K. V. Petrikov
View author publications
You can also search for this author in PubMed Google Scholar
Ya. A. Delegan
View author publications
You can also search for this author in PubMed Google Scholar
A. K. Surin
View author publications
You can also search for this author in PubMed Google Scholar
D. Linklater
View author publications
You can also search for this author in PubMed Google Scholar
A. E. Filonov
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. N. Ponamoreva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 460 KB)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Luong, T.M., Ponamoreva, O.N., Nechaeva, I.A. et al. Characterization of biosurfactants produced by the oil-degrading bacterium Rhodococcus erythropolis S67 at low temperature. World J Microbiol Biotechnol 34, 20 (2018). https://doi.org/10.1007/s11274-017-2401-8

Download citation

Received: 07 October 2017
Accepted: 13 December 2017
Published: 04 January 2018
DOI: https://doi.org/10.1007/s11274-017-2401-8

Keywords

Low-temperature biodegradation
Biosurfactants
Oil-degrading bacterium
Rhodococcus
Trehalose lipid