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Trehalose lipid biosurfactants produced by the actinomycetes Tsukamurella spumae and T. pseudospumae

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Abstract

Actinomycetales are known to produce various secondary metabolites including products with surface-active and emulsifying properties known as biosurfactants. In this study, the nonpathogenic actinomycetes Tsukamurella spumae and Tsukamurella pseudospumae are described as producers of extracellular trehalose lipid biosurfactants when grown on sunflower oil or its main component glyceryltrioleate. Crude extracts of the trehalose lipids were purified using silica gel chromatography. The structure of the two trehalose lipid components (TL A and TL B) was elucidated using a combination of matrix-assisted laser desorption/ionization time-of-flight/time-of-flight/tandem mass spectroscopy (MALDI-ToF-ToF/MS/MS) and multidimensional NMR experiments. The biosurfactants were identified as 1-α-glucopyranosyl-1-α-glucopyranosid carrying two acyl chains varying of C4 to C6 and C16 to C18 at the 2′ and 3′ carbon atom of one sugar unit. The trehalose lipids produced demonstrate surface-active behavior and emulsifying capacity. Classified as risk group 1 organisms, T. spumae and T. pseudospumae hold potential for the production of environmentally friendly surfactants.

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References

  • Asselineau C, Asselineau J (1978) Trehalose-containing glycolipids. Prog Chem Fats Other Lipids 16:59–99

    Article  PubMed  CAS  Google Scholar 

  • Azuma M, Suzutani T, Sazaki K, Yoshida I, Sakuma T, Yoshida T (1987) Role of interferon in the augmented resistance of trehalose-6, 6′-dimycolate-treated mice to influenza virus infection. J Gen Virol 68:835–843

    Article  PubMed  CAS  Google Scholar 

  • Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8(5):557–563

    Article  PubMed  CAS  Google Scholar 

  • Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58(1):1–26

    Article  PubMed  CAS  Google Scholar 

  • Bicca FC, Fleck LC, Ayub MAZ (1999) Production of biosurfactant by hydrocarbon degrading Rhodococcus ruber and Rhodococcus erythropolis. Rev Microbiol 30(3):231–236

    Article  CAS  Google Scholar 

  • Cameotra SS, Makkar RS (2004) Recent applications of biosurfactants as biological and immunological molecules. Curr Opin Microbiol 7(3):262–266. doi:10.1016/j.mib.2004.04.006

    Article  PubMed  CAS  Google Scholar 

  • Choi KS, Kim SH, Lee TH (1999) Purification and characterization of biosurfactant from Tsukamurella sp. 26A. J Microbiol Biotechnol 9(1):32–38

    CAS  Google Scholar 

  • Christofi N, Ivshina I (2002) Microbial surfactants and their use in field studies of soil remediation. J Appl Microbiol 93(6):915–929

    Article  PubMed  CAS  Google Scholar 

  • Daniel H-J, Reuss M, Syldatk C (1998) Production of sophorolipids in high concentration from deproteinized whey and rapeseed oil in a two stage fed batch process using Candida bombicola ATCC 22214 and Cryptococcus curvatus ATCC 20509. Biotechnol Lett 20(12):1153–1156. doi:10.1023/a:1005332605003

    Article  CAS  Google Scholar 

  • Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61(1):47–64

    PubMed  CAS  PubMed Central  Google Scholar 

  • DSMZ (webpage) Leibnitz Institute—German collection of microorganisms and cell cultures, catalogue of microorganisms. http://www.dsmz.de/catalogues/details/culture/DSM-44113.html Accessed: 23.05.2014

  • Du Noüy PL (1919) A new apparatus for measuring surface tension. J Gen Physiol 1(5):521

    Article  PubMed  PubMed Central  Google Scholar 

  • Embley T, Stackebrandt E (1994) The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 48(1):257–289

    Article  PubMed  CAS  Google Scholar 

  • Franzetti A, Gandolfi I, Bestetti G, Smyth TJ, Banat IM (2010) Production and applications of trehalose lipid biosurfactants. Eur J Lipid Sci Technol 112(6):617–627

    Article  CAS  Google Scholar 

  • Gudiña EJ, Rangarajan V, Sen R, Rodrigues LR (2013) Potential therapeutic applications of biosurfactants. Trends Pharmacol Sci 34(12):667–675

    Article  PubMed  Google Scholar 

  • Henkel M, Müller MM, Kügler JH, Lovaglio RB, Contiero J, Syldatk C, Hausmann R (2012) Rhamnolipids as biosurfactants from renewable resources: concepts for next-generation rhamnolipid production. Process Biochem 47(8):1207–1219

    Article  CAS  Google Scholar 

  • Iwahori K, Tokutomi T, Miyata N, Fujita M (2001) Formation of stable foam by the cells and culture supernatant of Gordonia (Nocardia) amarae. J Biosci Bioeng 92(1):77–79

    Article  PubMed  CAS  Google Scholar 

  • Jackisch-Matsuura AB, Santos LS, Eberlin MN, AiFd F, Matsuura T, Grossman MJ, Durrant LR (2014) Production and characterization of surface-active compounds from Gordonia amicalis. Braz Arch Biol Technol 57(1):138–144

    Article  CAS  Google Scholar 

  • Khopade A, Ren B, Liu X-Y, Mahadik K, Zhang L, Kokare C (2011) Production and characterization of biosurfactant from marine Streptomyces species B3. J Colloid Interface Sci 367(1):311–318

    Article  PubMed  Google Scholar 

  • Kim SH, Lim EJ, Lee SO, Lee JD, Lee TH (2000) Purification and characterization of biosurfactants from Nocardia sp. L-417. Biotechnol Appl Biochem 31(3):249–253

  • Kiran GS, Thomas TA, Selvin J (2010) Production of a new glycolipid biosurfactant from marine Nocardiopsis lucentensis MSA04 in solid-state cultivation. Colloids Surf B 78(1):8–16. doi:10.1016/j.colsurfb.2010.01.028

    Article  CAS  Google Scholar 

  • Kuyukina MS, Ivshina IB (2010) Application of Rhodococcus in bioremediation of contaminated environments. In: Alvarez HM (ed) Biology of Rhodococcus. Springer, Berlin, pp 231–262

  • Lang S, Philp JC (1998) Surface-active lipids in rhodococci. Anton Leeuw 74(1–3):59–70

  • Marat K Spinworks 3.1.8. University of Manitoba ftp://davinci.chem.umanitoba.ca/pub/marat/SpinWorks/

  • Marchant R, Banat IM (2012) Microbial biosurfactants: challenges and opportunities for future exploitation. Trends Biotechnol 30(11):558–565. doi:10.1016/j.tibtech.2012.07.003

    Article  PubMed  CAS  Google Scholar 

  • Morikawa M, Daido H, Takao T, Murata S, Shimonishi Y, Imanaka T (1993) A new lipopeptide biosurfactant produced by Arthrobacter sp. strain MIS38. J Bacteriol 175(20):6459–6466

    PubMed  CAS  PubMed Central  Google Scholar 

  • Müller MM, Kügler JH, Henkel M, Gerlitzki M, Hörmann B, Pöhnlein M, Syldatk C, Hausmann R (2012) Rhamnolipids—next generation surfactants? J Biotechnol 162(4):366–380

    Article  PubMed  Google Scholar 

  • Nam S-W, Chun J, Kim S, Kim W, Zakrzewska-Czerwinska J, Goodfellow M (2003) Tsukamurella spumae sp. nov., a novel actinomycete associated with foaming in activated sludge plants. Syst Appl Microbiol 26(3):367–375. doi:10.1078/072320203322497392

    Article  PubMed  CAS  Google Scholar 

  • Nam S-W, Kim W, Chun J, Goodfellow M (2004) Tsukamurella pseudospumae sp. nov., a novel actinomycete isolated from activated sludge foam. Int J Syst Evol Microbiol 54(4):1209–1212

    Article  PubMed  CAS  Google Scholar 

  • Niescher S, Wray V, Lang S, Kaschabek SR, Schlömann M (2006) Identification and structural characterisation of novel trehalose dinocardiomycolates from n-alkane-grown Rhodococcus opacus 1CP. Appl Microbiol Biotechnol 70(5):605–611

    Article  PubMed  CAS  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(2–3):318–324

    PubMed  CAS  Google Scholar 

  • Powalla M, Lang S, Wray V (1989) Penta- and disaccharide lipid formation by Nocardia corynebacteroides grown on n-alkanes. Appl Microbiol Biotechnol 31(5–6):473–479

    Article  CAS  Google Scholar 

  • Richter M, Willey JM, Süßmuth R, Jung G, Fiedler H-P (1998) Streptofactin, a novel biosurfactant with aerial mycelium inducing activity from Streptomyces tendae Tü 901/8c. FEMS Microbiol Lett 163(2):165–171. doi:10.1111/j.1574-6968.1998.tb13041.x

    CAS  Google Scholar 

  • Ristau E, Wagner F (1983) Formation of novel anionic trehalosetetraesters from Rhodococcus erythropolis under growth limiting conditions. Biotechnol Lett 5(2):95–100

    Article  CAS  Google Scholar 

  • Shao Z (2011) Trehalolipids. In: Soberón-Chávez G (ed) Biosurfactants—from genes to applications. Springer Berlin Heidelberg, pp 121-143

  • Sudo T, Zhao X, Wakamatsu Y, Shibahara M, Nomura N, Nakahara T, Suzuki A, Kobayashi Y, Jin C, Murata T (2000) Induction of the differentiation of human HL-60 promyelocytic leukemia cell line by succinoyl trehalose lipids. Cytotechnology 33(1–3):259–264

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tokumoto Y, Nomura N, Uchiyama H, Imura T, Morita T, Fukuoka T, Kitamoto D (2008) Structural characterization and surface-active properties of a succinoyl trehalose lipid produced by Rhodococcus sp. SD-74. J Oleo Sci 58(2):97–102

    Article  Google Scholar 

  • Vollbrecht E, Heckmann R, Wray V, Nimtz M, Lang S (1998) Production and structure elucidation of di- and oligosaccharide lipids (biosurfactants) from Tsukamurella sp. nov. Appl Microbiol Biotechnol 50(5):530–537

    Article  PubMed  CAS  Google Scholar 

  • Watanabe R, Yoo YC, Hata K, Mitobe M, Koike Y, Nishizawa M, Garcia DM, Nobuchi Y, Imagawa H, Yamada H (1999) Inhibitory effect of trehalose dimycolate (TDM) and its stereoisometric derivatives, trehalose dicorynomycolates (TDCMs), with low toxicity on lung metastasis of tumour cells in mice. Vaccine 17(11):1484–1492

    Article  PubMed  CAS  Google Scholar 

  • Zaragoza A, Aranda FJ, Espuny MJ, Teruel JA, Marqués A, Manresa A, Ortiz A (2009) Mechanism of membrane permeabilization by a bacterial trehalose lipid biosurfactant produced by Rhodococcus sp. Langmuir 25(14):7892–7898

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the German Federal Ministry of Education and Research for funding this project (0315928B) as part of the ERA-IB BioSurf project (617 4003 0315928B).

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Authors and Affiliations

  1. Institute of Process Engineering in Life Sciences, Section II: Technical Biology, Karlsruhe Institute of Technology (KIT), Engler-Bunte Ring 1, 76131, Karlsruhe, Germany

    Johannes H. Kügler, Axel Kraft, Raphael Heinzler, Marius Henkel & Christoph Syldatk

  2. Institute of Organic Chemistry, Karlsruhe Institute of Technology (KIT), Fritz-Haber Weg 6, 76131, Karlsruhe, Germany

    Claudia Muhle-Goll & Burkhard Luy

  3. Institute of Functional Interfaces, Department Microbiology of Natural and Technical Interfaces, Karlsruhe Institute of Technology (KIT), Hermann von Helmholtz Platz 1, 76344, Eggenstein-Leopoldshafen, Germany

    Boris Kühl, Frank Kirschhöfer & Gerald Brenner-Weiss

  4. Department of Molecular Structural Biology, Helmholtz Centre for Infection Research, Inhoffenstr. 7, 38124, Braunschweig, Germany

    Victor Wray

  5. Institute for Biological Interfaces, Karlsruhe Institute of Technology (KIT), Hermann-von-Helmholtz-Platz 1, 76344, Eggenstein-Leopoldshafen, Germany

    Burkhard Luy

  6. Institute for Biochemistry, Biotechnology and Bioinformatics, Department of Biotechnology, Technical University Braunschweig, Spielmannstraße 7, 38106, Braunschweig, Germany

    Siegmund Lang

  7. Institute of Food Science and Biotechnology, Section Bioprocess Engineering, University of Hohenheim, Garbenstr. 25, 70599, Stuttgart, Germany

    Rudolf Hausmann

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  1. Johannes H. Kügler
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  2. Claudia Muhle-Goll
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  3. Boris Kühl
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  7. Marius Henkel
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  8. Victor Wray
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  9. Burkhard Luy
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  10. Gerald Brenner-Weiss
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  11. Siegmund Lang
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  12. Christoph Syldatk
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  13. Rudolf Hausmann
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Corresponding author

Correspondence to Johannes H. Kügler.

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Kügler, J.H., Muhle-Goll, C., Kühl, B. et al. Trehalose lipid biosurfactants produced by the actinomycetes Tsukamurella spumae and T. pseudospumae . Appl Microbiol Biotechnol 98, 8905–8915 (2014). https://doi.org/10.1007/s00253-014-5972-4

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  • DOI: https://doi.org/10.1007/s00253-014-5972-4

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