Applied Microbiology and Biotechnology

, Volume 98, Issue 21, pp 8905–8915 | Cite as

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

  • Johannes H. Kügler
  • Claudia Muhle-Goll
  • Boris Kühl
  • Axel Kraft
  • Raphael Heinzler
  • Frank Kirschhöfer
  • Marius Henkel
  • Victor Wray
  • Burkhard Luy
  • Gerald Brenner-Weiss
  • Siegmund Lang
  • Christoph Syldatk
  • Rudolf Hausmann
Biotechnological products and process engineering

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.

Keywords

Trehalose lipid Biosurfactant Surfactant Bioemulsifier Emulsifier Tsukamurella Actinomycete 

Supplementary material

253_2014_5972_MOESM1_ESM.pdf (543 kb)
ESM 1(PDF 543 kb)

References

  1. Asselineau C, Asselineau J (1978) Trehalose-containing glycolipids. Prog Chem Fats Other Lipids 16:59–99PubMedCrossRefGoogle Scholar
  2. 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 68:835–843PubMedCrossRefGoogle Scholar
  3. Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8(5):557–563PubMedCrossRefGoogle Scholar
  4. Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58(1):1–26PubMedCrossRefGoogle Scholar
  5. Bicca FC, Fleck LC, Ayub MAZ (1999) Production of biosurfactant by hydrocarbon degrading Rhodococcus ruber and Rhodococcus erythropolis. Rev Microbiol 30(3):231–236CrossRefGoogle Scholar
  6. 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 PubMedCrossRefGoogle Scholar
  7. Choi KS, Kim SH, Lee TH (1999) Purification and characterization of biosurfactant from Tsukamurella sp. 26A. J Microbiol Biotechnol 9(1):32–38Google Scholar
  8. Christofi N, Ivshina I (2002) Microbial surfactants and their use in field studies of soil remediation. J Appl Microbiol 93(6):915–929PubMedCrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61(1):47–64PubMedPubMedCentralGoogle Scholar
  11. 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
  12. Du Noüy PL (1919) A new apparatus for measuring surface tension. J Gen Physiol 1(5):521PubMedCrossRefPubMedCentralGoogle Scholar
  13. Embley T, Stackebrandt E (1994) The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 48(1):257–289PubMedCrossRefGoogle Scholar
  14. 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):617–627CrossRefGoogle Scholar
  15. Gudiña EJ, Rangarajan V, Sen R, Rodrigues LR (2013) Potential therapeutic applications of biosurfactants. Trends Pharmacol Sci 34(12):667–675PubMedCrossRefGoogle Scholar
  16. 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):1207–1219CrossRefGoogle Scholar
  17. 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):77–79PubMedCrossRefGoogle Scholar
  18. 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):138–144CrossRefGoogle Scholar
  19. 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):311–318PubMedCrossRefGoogle Scholar
  20. 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):249–253Google Scholar
  21. 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 CrossRefGoogle Scholar
  22. Kuyukina MS, Ivshina IB (2010) Application of Rhodococcus in bioremediation of contaminated environments. In: Alvarez HM (ed) Biology of Rhodococcus. Springer, Berlin, pp 231–262Google Scholar
  23. Lang S, Philp JC (1998) Surface-active lipids in rhodococci. Anton Leeuw 74(1–3):59–70Google Scholar
  24. Marat K Spinworks 3.1.8. University of Manitoba ftp://davinci.chem.umanitoba.ca/pub/marat/SpinWorks/
  25. 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 PubMedCrossRefGoogle Scholar
  26. 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):6459–6466PubMedPubMedCentralGoogle Scholar
  27. 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):366–380PubMedCrossRefGoogle Scholar
  28. 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 PubMedCrossRefGoogle Scholar
  29. 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):1209–1212PubMedCrossRefGoogle Scholar
  30. 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):605–611PubMedCrossRefGoogle Scholar
  31. 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):318–324PubMedGoogle Scholar
  32. 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):473–479CrossRefGoogle Scholar
  33. 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 Google Scholar
  34. Ristau E, Wagner F (1983) Formation of novel anionic trehalosetetraesters from Rhodococcus erythropolis under growth limiting conditions. Biotechnol Lett 5(2):95–100CrossRefGoogle Scholar
  35. Shao Z (2011) Trehalolipids. In: Soberón-Chávez G (ed) Biosurfactants—from genes to applications. Springer Berlin Heidelberg, pp 121-143Google Scholar
  36. 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):259–264PubMedCrossRefPubMedCentralGoogle Scholar
  37. 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):97–102CrossRefGoogle Scholar
  38. 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):530–537PubMedCrossRefGoogle Scholar
  39. 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):1484–1492PubMedCrossRefGoogle Scholar
  40. 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):7892–7898PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Johannes H. Kügler
    • 1
  • Claudia Muhle-Goll
    • 2
  • Boris Kühl
    • 3
  • Axel Kraft
    • 1
  • Raphael Heinzler
    • 1
  • Frank Kirschhöfer
    • 3
  • Marius Henkel
    • 1
  • Victor Wray
    • 4
  • Burkhard Luy
    • 2
    • 5
  • Gerald Brenner-Weiss
    • 3
  • Siegmund Lang
    • 6
  • Christoph Syldatk
    • 1
  • Rudolf Hausmann
    • 7
  1. 1.Institute of Process Engineering in Life Sciences, Section II: Technical BiologyKarlsruhe Institute of Technology (KIT)KarlsruheGermany
  2. 2.Institute of Organic ChemistryKarlsruhe Institute of Technology (KIT)KarlsruheGermany
  3. 3.Institute of Functional Interfaces, Department Microbiology of Natural and Technical InterfacesKarlsruhe Institute of Technology (KIT)Eggenstein-LeopoldshafenGermany
  4. 4.Department of Molecular Structural BiologyHelmholtz Centre for Infection ResearchBraunschweigGermany
  5. 5.Institute for Biological InterfacesKarlsruhe Institute of Technology (KIT)Eggenstein-LeopoldshafenGermany
  6. 6.Institute for Biochemistry, Biotechnology and Bioinformatics, Department of BiotechnologyTechnical University BraunschweigBraunschweigGermany
  7. 7.Institute of Food Science and Biotechnology, Section Bioprocess EngineeringUniversity of HohenheimStuttgartGermany

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