Skip to main content
SpringerLink
Log in

The production, properties, and applications of thermostable steryl glucosidases

  • Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Extremophilic microorganisms are a rich source of enzymes, the enzymes which can serve as industrial catalysts that can withstand harsh processing conditions. An example is thermostable β-glucosidases that are addressing a challenging problem in the biodiesel industry: removing steryl glucosides (SGs) from biodiesel. Steryl glucosidases (SGases) must be tolerant to heat and solvents in order to function efficiently in biodiesel. The amphipathic nature of SGs also requires enzymes with an affinity for water/solvent interfaces in order to achieve efficient hydrolysis. Additionally, the development of an enzymatic process involving a commodity such as soybean biodiesel must be cost-effective, necessitating an efficient manufacturing process for SGases. This review summarizes the identification of microbial SGases and their applications, discusses biodiesel refining processes and the development of analytical methods for identifying and quantifying SGs in foods and biodiesel, and considers technologies for strain engineering and process optimization for the heterologous production of a SGase from Thermococcus litoralis. All of these technologies might be used for the production of other thermostable enzymes. Structural features of SGases and the feasibility of protein engineering for novel applications are explored.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams MW, Perler FB, Kelly RM (1995) Extremozymes: expanding the limits of biocatalysis. Nat Biotechnol 13:662–668

    Article  CAS  Google Scholar 

  • Aguirre A, Peiru S, Eberhardt F, Vetcher L, Cabrera R, Menzella HG (2014) Enzymatic hydrolysis of steryl glucosides, major contaminants of vegetable oil-derived biodiesel. Appl Microbiol Biotechnol 98:4033–4040. https://doi.org/10.1007/s00253-013-5345-4

    Article  CAS  Google Scholar 

  • Aguirre A, Cabruja M, Cabrera R, Eberhardt F, Peirú S, Menzella HG, Rasia RM (2015) A fluorometric enzymatic assay for quantification of steryl glucosides in biodiesel. J Am Oil Chem Soc 92:47–53

    Article  CAS  Google Scholar 

  • Akiba T, Nishio M, Matsui I, Harata K (2004) X-ray structure of a membrane-bound beta-glycosidase from the hyperthermophilic archaeon Pyrococcus horikoshii. Proteins 57:422–431. https://doi.org/10.1002/prot.20203

    Article  CAS  Google Scholar 

  • Aloulou A, Rodriguez JA, Fernandez S, van Oosterhout D, Puccinelli D, Carrière F (2006) Exploring the specific features of interfacial enzymology based on lipase studies. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids 1761:995–1013

    Article  CAS  Google Scholar 

  • Al-Zuhair S, Ramachandran K, Hasan M (2008) Effect of enzyme molecules covering of oil–water interfacial area on the kinetic of oil hydrolysis. Chem Eng J 139:540–548

    Article  CAS  Google Scholar 

  • An DS et al (2010) Identification and characterization of a novel Terrabacter ginsenosidimutans sp. nov. beta-glucosidase that transforms ginsenoside Rb1 into the rare gypenosides XVII and LXXV. Appl Environ Microbiol 76:5827–5836. https://doi.org/10.1128/AEM.00106-10AEM.00106-10

    Article  CAS  Google Scholar 

  • Anbarasan S, Timoharju T, Barthomeuf J, Pastinen O, Rouvinen J, Leisola M, Turunen O (2015) Effect of active site mutation on pH activity and transglycosylation of Sulfolobus acidocaldarius β-glycosidase. J Mol Catal B: Enzym 118:62–69

    Article  CAS  Google Scholar 

  • Badenes SM, Lemos F, Cabral JM (2011) Kinetics and mechanism of the cutinase-catalyzed transesterification of oils in AOT reversed micellar system. Bioprocess Biosyst Eng 34:1133–1142

    Article  CAS  Google Scholar 

  • Bernaudat F et al. (2011) Heterologous expression of membrane proteins: choosing the appropriate host. PLoS ONE 6:e29191

    Article  CAS  Google Scholar 

  • Bouic PJ, Etsebeth S, Liebenberg RW, Albrecht CF, Pegel K, Van Jaarsveld PP (1996) beta-Sitosterol and beta-sitosterol glucoside stimulate human peripheral blood lymphocyte proliferation: implications for their use as an immunomodulatory vitamin combination. Int J Immunopharmacol 18:693–700

    Article  CAS  Google Scholar 

  • Brask J, Nielsen R (2010) Enzymatic removal of steryl glycosides in fatty acid alkyl esters WO2010102952 A1

  • Camerlynck S, Chandler J, Hornby B, van Zuylen I (2012) FAME filterability: understanding and solutions SAE. Int J Fuels Lubr 5:968–976

    Article  CAS  Google Scholar 

  • Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859 https://doi.org/10.1016/S0969-2126(01)00220-9

    Article  CAS  Google Scholar 

  • Deive FJ, López E, Rodriguez A, Longo MA, Sanromán M (2012) Targeting the production of biomolecules by extremophiles at bioreactor scale. Chem Eng Technol 35:1565–1575

    Article  CAS  Google Scholar 

  • Doukyu N, Ogino H (2010) Organic solvent-tolerant enzymes. Biochem Eng J 48:270–282

    Article  CAS  Google Scholar 

  • Eberhardt F, Aguirre A, Menzella HG, Peiru S (2017) Strain engineering and process optimization for enhancing the production of a thermostable steryl glucosidase in Escherichia coli. J Ind Microbiol Biotechnol 44:141–147. https://doi.org/10.1007/s10295-016-1866-z

    Article  CAS  Google Scholar 

  • Eberhardt F et al. (2018) Pilot-scale process development for low-cost production of a thermostable biodiesel refining enzyme in Escherichia coli. Bioprocess Biosyst Eng 1–10

  • Elleuche S, Schroder C, Sahm K, Antranikian G (2014) Extremozymes–biocatalysts with unique properties from extremophilic microorganisms. Curr Opin Biotechnol 29:116–123. https://doi.org/10.1016/j.copbio.2014.04.003

    Article  CAS  Google Scholar 

  • Gómez-Coca RB, Pérez-Camino MdC, Moreda W (2012) Specific procedure for analysing steryl glucosides in olive oil European. J Lipid Sci Technol 114:1417–1426

    Article  Google Scholar 

  • Gupta A, Khare S (2009) Enzymes from solvent-tolerant microbes: useful biocatalysts for non-aqueous enzymology. Crit Rev Biotechnol 29:44–54

    Article  CAS  Google Scholar 

  • Hermansyah H, Kubo M, Shibasaki-Kitakawa N, Yonemoto T (2006) Mathematical model for stepwise hydrolysis of triolein using Candida rugosa lipase in biphasic oil–water system. Biochem Eng J 31:125–132

    Article  CAS  Google Scholar 

  • Hermansyah H, Wijanarko A, Kubo M, Shibasaki-Kitakawa N, Yonemoto T (2010) Rigorous kinetic model considering positional specificity of lipase for enzymatic stepwise hydrolysis of triolein in biphasic oil–water system. Bioprocess Biosyst Eng 33:787–796

    Article  CAS  Google Scholar 

  • Isorna P, Polaina J, Latorre-Garcia L, Canada FJ, Gonzalez B, Sanz-Aparicio J (2007) Crystal structures of Paenibacillus polymyxa beta-glucosidase B complexes reveal the molecular basis of substrate specificity and give new insights into the catalytic machinery of family I glycosidases. J Mol Biol 371:1204–1218. https://doi.org/10.1016/j.jmb.2007.05.082

    Article  CAS  Google Scholar 

  • Junge F, Schneider B, Reckel S, Schwarz D, Dötsch V, Bernhard F (2008) Large-scale production of functional membrane proteins. Cell Mol Life Sci 65:1729–1755

    Article  CAS  Google Scholar 

  • Kalinowska M, Wojciechowski ZA (1978) Purification and some properties of steryl beta-D-glucoside hydrolase from Sinapis alba seedlings. Phytochemistry 17:1533–1537

    Article  CAS  Google Scholar 

  • Lacoste F, Dejean F, Griffon H, Rouquette C (2009) Quantification of free and esterified steryl glucosides in vegetable oils and biodiesel European. J Lipid Sci Technol 111:822–828. https://doi.org/10.1002/ejlt.200800297

    Article  CAS  Google Scholar 

  • Lee I, Pfalzgraf L, Poppe G, Powers E, Haines T (2007) The role of sterol glucosides on filter plugging. Biodiesel Mag 4:105–112

    Google Scholar 

  • Leung DY, Wu X, Leung M (2010) A review on biodiesel production using catalyzed transesterification. Appl Energy 87:1083–1095

    Article  CAS  Google Scholar 

  • Lin X, Ma L, Racette SB, Anderson Spearie CL, Ostlund RE Jr (2009) Phytosterol glycosides reduce cholesterol absorption in humans. Am J Physiol Gastrointest Liver Physiol 296:G931-935. https://doi.org/10.1152/ajpgi.00001.2009

    Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2013) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495

    Article  Google Scholar 

  • Matsui I, Sakai Y, Matsui E, Kikuchi H, Kawarabayasi Y, Honda K (2000) Novel substrate specificity of a membrane-bound beta-glycosidase from the hyperthermophilic archaeon Pyrococcus horikoshii. FEBS Lett 467:195–200

    Article  CAS  Google Scholar 

  • Menzella H, Peiru S, Vetcher L (2012) Enzymatic Removal of Steryl Glycosides PCT/US2013/031769

  • Middelberg AP, O’Neill BK, ID LB, Snoswell MA (1991) A novel technique for the measurement of disruption in high-pressure homogenization: studies on E. coli containing recombinant inclusion bodies. Biotechnol Bioeng 38:363–370. https://doi.org/10.1002/bit.260380406

    Article  CAS  Google Scholar 

  • Miroux B, Walker JE (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260(3):289–298

    Article  CAS  Google Scholar 

  • Munger LH, Nystrom L (2014) Enzymatic hydrolysis of steryl glycosides for their analysis in foods. Food Chem 163:202–211. https://doi.org/10.1016/j.foodchem.2014.04.082

    Article  CAS  Google Scholar 

  • Na-Ranong D, Kitchaiya P (2014) Precipitation above cloud point in palm oil based biodiesel during production and storage. Fuel 122:287–293. https://doi.org/10.1016/j.fuel.2014.01.003

    Article  CAS  Google Scholar 

  • Noh KH, Oh DK (2009) Production of the rare ginsenosides compound K, compound Y, and compound Mc by a thermostable beta-glycosidase from Sulfolobus acidocaldarius. Biol Pharm Bull 32:1830–1835

    Article  CAS  Google Scholar 

  • Noh KH, Son JW, Kim HJ, Oh DK (2009) Ginsenoside compound K production from ginseng root extract by a thermostable beta-glycosidase from Sulfolobus solfataricus. Biosci Biotechnol Biochem 73:316–321

    Article  CAS  Google Scholar 

  • Nystrom L (2008) Enzymatic hydrolisis of steryl ferulates and steryl glycosides. Eur Food Res Technol 227:727–733

    Article  CAS  Google Scholar 

  • Oppliger SR, Munger LH, Nystrom L (2014) Rapid and highly accurate detection of steryl glycosides by ultraperformance liquid chromatography-quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF-MS). J Agric Food Chem 62:9410–9419. https://doi.org/10.1021/jf501509m

    Article  CAS  Google Scholar 

  • Peiru S, Aguirre A, Eberhardt F, Braia M, Cabrera R, Menzella HG (2015) An industrial scale process for the enzymatic removal of steryl glucosides from biodiesel. Biotechnol Biofuels 8:223. https://doi.org/10.1186/s13068-015-0405-x

    Article  Google Scholar 

  • Pfalzgraf L, Lee I, Foster J, Poppe G (2007) The effect of minor components on cloud point and filterability inform. Suppl Biorenewable Resour 4:17–21

    Google Scholar 

  • Plata V, Gauthier-Maradei P, Kafarov V (2014) Influence of minor components on precipitate formation and filterability of palm oil biodiesel. Fuel 144:130–136

    Article  Google Scholar 

  • Reis P, Holmberg K, Watzke H, Leser M, Miller R (2009) Lipases at interfaces: a review. Adv Colloid Interface Sci 147:237–250

    Article  Google Scholar 

  • Ringwald SC (2007) Biodiesel characterization in the QC environment. The 98th AOCS Annual Meeting Abstracts AOCS Press, Urbana:15

  • Rozzell JD (1999) Commercial scale biocatalysis: myths and realities. Bioorg Med Chem 7:2253–2261

    Article  CAS  Google Scholar 

  • Sarmiento F, Peralta R, Blamey JM (2015) Cold and hot extremozymes: industrial relevance and current trends. Front Bioeng Biotechnol 3:148 https://doi.org/10.3389/fbioe.2015.00148

    Article  Google Scholar 

  • Schröter S, Stahmann K-P, Schnitzlein K (2015) Impact of mass transport on the enzymatic hydrolysis of rapeseed oil. Appl Microbiol Biotechnol 99:293–300

    Article  Google Scholar 

  • Soe JB (2010) Method WO 2010004423 p A2

  • Sugawara T, Miyazawa T (1999) Separation and determination of glycolipids from edible plant sources by high-performance liquid chromatography and evaporative light- scattering detection Lipids 34:1231–1237

    Article  CAS  Google Scholar 

  • Tang H, De Guzman R, Salley S, Simon Ng KY (2010) Comparing process efficiency in reducing steryl glucosides in biodiesel. J Am Oil Chem Soc 87:337–345

    Article  CAS  Google Scholar 

  • Umetsu M, Tsumoto K, Ashish K, Nitta S, Tanaka Y, Adschiri T, Kumagai I (2004) Structural characteristics and refolding of in vivo aggregated hyperthermophilic archaeon proteins. FEBS Lett 557:49–56

    Article  CAS  Google Scholar 

  • Van Hoed V, Zyaykina N, de Greyt W, Maes J, Verhé R, Demeestere K (2008) Identification and occurrence of steryl glucosides in palm and soy biodiesel. J Am Oil Chem Soc 85:701–709

    Article  Google Scholar 

  • Verger R, De Haas GH (1976) Interfacial enzyme kinetics of lipolysis. Ann Rev Biophys Bioeng 5:77–117

    Article  CAS  Google Scholar 

  • Webb B, Sali A (2014) Protein structure modeling with MODELLER. In: Protein structure prediction. Springer, New York, pp 1–15

    Google Scholar 

Download references

Funding

The funding was provided by ANCYT PICT (Grant Nos. 2010-1157, 2013-2134, 2013-2726).

Author information

Authors and Affiliations

  1. Instituto de Procesos Biotecnológicos y Químicos (IPROBYQ), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), CONICET, Suipacha 531, 2000, Rosario, Argentina

    Andres Aguirre, Florencia Eberhardt, Guillermo Hails, Sebastian Cerminati, María Eugenia Castelli, Luciana Paoletti, Hugo G. Menzella & Salvador Peiru

  2. Keclon S.A., Tucuman 7180, 2000, Rosario, Argentina

    Andres Aguirre, Hugo G. Menzella & Salvador Peiru

  3. Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET-UNR), Area Biofísica, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Ocampo y Esmeralda, predio CONICET, Rosario, 2000, Argentina

    Rodolfo M. Rasia

Authors
  1. Andres Aguirre
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Florencia Eberhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillermo Hails
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sebastian Cerminati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. María Eugenia Castelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rodolfo M. Rasia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luciana Paoletti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hugo G. Menzella
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Salvador Peiru
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Salvador Peiru.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aguirre, A., Eberhardt, F., Hails, G. et al. The production, properties, and applications of thermostable steryl glucosidases. World J Microbiol Biotechnol 34, 40 (2018). https://doi.org/10.1007/s11274-018-2423-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-018-2423-x

Keywords

Search

Navigation