Abstract
Certain members of the carboxylesterase superfamily can act at the interface between water and water-insoluble substrates. However, nonnatural bulky polyesters usually are not efficiently hydrolyzed. In the recent years, the potential of enzyme engineering to improve hydrolysis of synthetic polyesters has been demonstrated. Regions on the enzyme surface have been modified by using site-directed mutagenesis in order to tune sorption processes through increased hydrophobicity of the enzyme surface. Such modifications can involve specific amino acid substitutions, addition of binding modules, or truncation of entire domains improving sorption properties and/or dynamics of the enzyme. In this review, we provide a comprehensive overview on different strategies developed in the recent years for enzyme surface engineering to improve the activity of polyester-hydrolyzing enzymes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amass W, Amass A, Tighe B (1998) A review of biodegradable polymers: uses, current developments in the synthesis and characterization of biodegradable polyesters, blends of biodegradable polymers and recent advances in biodegradation studies. Polym Int 47:89–144. https://doi.org/10.1002/(SICI)1097-0126(1998100)47:2<89::AID-PI86>3.0.CO;2-F
Anobom CD, Pinheiro AS, De-Andrade RA, Aguieiras ECG, Andrade GC, Moura MV, Almeida RV, Freire DM (2014) From structure to catalysis: recent developments in the biotechnological applications of lipases. Biomed Res Int 2014:684506–684511. https://doi.org/10.1155/2014/684506
Araújo R, Silva C, O’Neill A, Micaelo N, Guebitz G, Soares CM, Casal M, Cavaco-Paulo A (2007) Tailoring cutinase activity towards polyethylene terephthalate and polyamide 6,6 fibers. J Biotechnol 128:849–857. https://doi.org/10.1016/j.jbiotec.2006.12.028
Arpigny JL, Jaeger KE (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343(Pt 1):177–183
Baker PJ, Poultney C, Liu Z, Gros R, Montclare JK (2012) Identification and comparison of cutinases for synthetic polyester degradation. Appl Microbiol Biotechnol 93(1):229–240. https://doi.org/10.1007/s00253-011-3402-4
Biundo A, Ribitsch D, Steinkellner G, Gruber K, Guebitz GM (2016) Polyester hydrolysis is enhanced by a truncated esterase: less is more. Biotechnol J 12. https://doi.org/10.1002/biot.201600450
Biundo A, Steinkellner G, Gruber K, Spreitzhofer T, Ribitsch D, Guebitz GM, Gruber K, Schwab H, Guebitz GM, Golyshin PN, Savchenko A, Edwards EA, Yakunin AF, Acero EH, Guebitz GM, Schwab H, Guebitz GM (2017) Engineering of the zinc-binding domain of an esterase from clostridium botulinum towards increased activity on polyesters. Catal Sci Technol 7:1440–1447. https://doi.org/10.1039/C7CY00168A
Biundo A, Reich J, Ribitsch D, Gubitz GM (2018) Synergistic effect of mutagenesis and truncation to improve a polyesterase from Clostridium botulinum for polyester hydrolysis. Sci Rep. Accepted
Brueckner T, Eberl A, Heumann S, Rabe M, Guebitz GM (2008) Enzymatic and chemical hydrolysis of poly(ethylene terephthalate) fabrics. J Polym Sci Part A Polym Chem 46:6435–6443. https://doi.org/10.1002/pola.22952
Carrasco-Lopez C, Godoy C, de las Rivas B, Fernandez-Lorente G, Palomo JM, Guisan JM, Fernandez-Lafuente R, Martinez-Ripoll M, Hermoso JA (2009) Activation of bacterial thermoalkalophilic lipases is spurred by dramatic structural rearrangements. J Biol Chem 284:4365–4372. https://doi.org/10.1074/jbc.M808268200
Chen S, Su L, Chen J, Wu J (2013) Cutinase: characteristics, preparation, and application. Biotechnol Adv 31:1754–1767. https://doi.org/10.1016/j.biotechadv.2013.09.005
Chen S, Liu Z, Chen J, Wu J (2011) Study on improvement of extracellular production of recombinant Thermobifida fusca cutinase by Escherichia coli. Appl Biochem Biotechnol 165(2):666–675. https://doi.org/10.1007/s12010-011-9286-z
Chica RA, Doucet N, Pelletier JN (2005) Semi-rational approaches to engineering enzyme activity: combining the benefits of directed evolution and rational design. Curr Opin Biotechnol 16:378–384. https://doi.org/10.1016/j.copbio.2005.06.004
Choi W-C, Kim MH, Ro H-S, Ryu SR, Oh T-K, Lee J-K (2005) Zinc in lipase L1 from Geobacillus stearothermophilus L1 and structural implications on thermal stability. FEBS Lett 579:3461–3466. https://doi.org/10.1016/j.febslet.2005.05.016
Dimarogona M, Nikolaivits E, Kanelli M, Christakopoulos P, Sandgren M, Topakas E (2015) Structural and functional studies of a Fusarium oxysporum cutinase with polyethylene terephthalate modification potential. Biochim Biophys Acta 1850(11):2308–2317. https://doi.org/10.1016/j.bbagen.2015.08.009
Donelli I, Taddei P, Smet PF, Poelman D, Nierstrasz VA, Freddi G (2009) Enzymatic surface modification and functionalization of PET: a water contact angle, FTIR, and fluorescence spectroscopy study. Biotechnol Bioeng 103:845–856. https://doi.org/10.1002/bit.22316
Donelli I, Freddi G, Nierstrasz VA, Taddei P (2010) Surface structure and properties of poly-(ethylene terephthalate) hydrolyzed by alkali and cutinase. Polym Degrad Stab 95:1542–1550. https://doi.org/10.1016/j.polymdegradstab.2010.06.011
Eberl A, Heumann S, Bruckner T, Araujo R, Cavaco-Paulo A, Kaufmann F, Kroutil W, Guebitz GM (2009) Enzymatic surface hydrolysis of poly(ethylene terephthalate) and bis(benzoyloxyethyl) terephthalate by lipase and cutinase in the presence of surface active molecules. J Biotechnol 143:207–212
Eberl A, Heumann S, Kotek R, Kaufmann F, Mitsche S, Cavaco-Paulo A, Gübitz GM (2008) Enzymatic hydrolysis of PTT polymers and oligomers. J Biotechnol 135(1):45–51
Espino-Rammer L, Ribitsch D, Przylucka A, Marold A, Greimel KJ, Herrero Acero E, Guebitz GM, Kubicek CP, Druzhinina IS (2013) Two novel class II hydrophobins from Trichoderma spp. stimulate enzymatic hydrolysis of poly(ethylene terephthalate) when expressed as fusion proteins. Appl Environ Microbiol 79:4230–4238. https://doi.org/10.1128/AEM.01132-13
Georg M. Guebitz, Enrique Herrero Acero, Karolina Härnvall, Patrick Fladischer, Georg Steinkellner, Birgit Willtschi, Karl Gruber, Helmut Schwab, Christian P. Kubicek, Irina S. Druzhinina DR (2013) Synthetic enzymes for synthetic polymers. In: The 6th Central European Conference - Chemistry Towards Biology
Gusakov AV, Berlin AG, Popova NN, Okunev ON, Sinitsyna OA, Sinitsyn AP (2000) A comparative study of different cellulase preparations in the enzymatic treatment of cotton fabrics. Appl Biochem Biotechnol 88:119–126. https://doi.org/10.1385/ABAB:88:1-3:119
Herrero Acero E, Ribitsch D, Steinkellner G, Gruber K, Greimel K, Eiteljoerg I, Trotscha E, Wei R, Zimmermann W, Zinn M, Cavaco-Paulo A, Freddi G, Schwab H, Guebitz G (2011) Enzymatic surface hydrolysis of PET: effect of structural diversity on kinetic properties of cutinases from Thermobifida. Macromolecules 44:4632–4640. https://doi.org/10.1021/ma200949p
Herrero Acero E, Ribitsch D, Dellacher A, Zitzenbacher S, Marold A, Steinkellner G, Gruber K, Schwab H, Guebitz GM (2013) Surface engineering of a cutinase from Thermobifida cellulosilytica for improved polyester hydrolysis. Biotechnol Bioeng 110:2581–2590. https://doi.org/10.1002/bit.24930
Jochens H, Hesseler M, Stiba K, Padhi SK, Kazlauskas RJ, Bornscheuer UT (2011) Protein engineering of α/β-hydrolase fold enzymes. Chembiochem 12:1508–1517. https://doi.org/10.1002/cbic.201000771
Kasuya K, Takano T, Tezuka Y, Hsieh WC, Mitomo H, Doi Y (2003) Cloning, expression and characterization of a poly(3-hydroxybutyrate) depolymerase from Marinobacter sp. NK-1. Int J Biol Macromol 33(4–5):221–226
Kawai F, Oda M, Tamashiro T, Waku T, Tanaka N, Yamamoto M, Mizushima H, Miyakawa T, Tanokura M (2014) A novel Ca2+−activated, thermostabilized polyesterase capable of hydrolyzing polyethylene terephthalate from Saccharomonospora viridis AHK190. Appl Microbiol Biotechnol 98:10053–10064. https://doi.org/10.1007/s00253-014-5860-y
Kern D, Eisenmesser EZ, Wolf-Watz M (2005) Enzyme dynamics during catalysis measured by NMR spectroscopy. In: Methods in enzymology. pp 507–524
Kobayashi S, Makino A (2009) Enzymatic polymer synthesis: an opportunity for green polymer chemistry. Chem Rev 109:5288–5353. https://doi.org/10.1021/cr900165z
Kontkanen H, Westerholm-Parvinen A, Saloheimo M, Bailey M, Rättö M, Mattila I, Mohsina M, Kalkkinen N, Nakari-Setälä T, Buchert J (2009) Novel Coprinopsis cinerea polyesterase that hydrolyzes cutin and suberin
Kontkanen H, Saloheimo M, Pere J, Miettinen-Oinonen A, Reinikainen T (2006) Characterization of Melanocarpus albomyces steryl esterase produced in Trichoderma reesei and modification of fibre products with the enzyme. Appl Microbiol Biotechnol 72(4):696–704
Liu Z, Gosser Y, Baker PJ, Ravee Y, Lu Z, Alemu G, Li H, Butterfoss GL, Kong XP, Gross R, Montclare JK (2009) Structural and functional studies of Aspergillus oryzae cutinase: enhanced thermostability and hydrolytic activity of synthetic ester and polyester degradation. J Am Chem Soc 131(43):15711–15716. https://doi.org/10.1021/ja9046697
Marten E, Müller R-J, Deckwer W-D (2005) Studies on the enzymatic hydrolysis of polyesters. II. Aliphatic–aromatic copolyesters. Polym Degrad Stab 88:371–381. https://doi.org/10.1016/j.polymdegradstab.2004.12.001
Muroi F, Tachibana Y, Soulenthone P, Yamamoto K, Mizuno T, Sakurai T, Kobayashi Y, Kasuya K (2017) Characterization of a poly(butylene adipate-co-terephthalate) hydrolase from the aerobic mesophilic bacterium Bacillus pumilus. Polym Degrad Stab 137:11–22 https://doi.org/10.1016/j.polymdegradstab.2017.01.006
Nardini M, Dijkstra BW (1999) Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 9:732–737
Neves Petersen MT, Fojan P, Petersen SB (2001) How do lipases and esterases work: the electrostatic contribution. J Biotechnol 85:115–147. https://doi.org/10.1016/S0168-1656(00)00360-6
Oeser T, Wei R, Baumgarten T, Billig S, Föllner C, Zimmermann W (2010) High level expression of a hydrophobic poly(ethylene terephthalate)-hydrolyzing carboxylesterase from Thermobifida fusca KW3 in Escherichia coli BL21(DE3). J Biotechnol 146(3):100–104. https://doi.org/10.1016/j.jbiotec.2010.02.006
Pellis A, Herrero Acero E, Ferrario V, Ribitsch D, Guebitz GM, Gardossi L (2016) The closure of the cycle: enzymatic synthesis and functionalization of bio-based polyesters. Trends Biotechnol 34:316–328. https://doi.org/10.1016/j.tibtech.2015.12.009
Perz V, Zumstein MT, Sander M, Zitzenbacher S, Ribitsch D, Guebitz GM (2015) Biomimetic approach to enhance enzymatic hydrolysis of the synthetic polyester poly(1,4-butylene adipate): fusing binding modules to Esterases. Biomacromolecules 16:3889–3896. https://doi.org/10.1021/acs.biomac.5b01219
Perz V, Hromic A, Baumschlager A, Steinkellner G, Pavkov-Keller T, Gruber K, Bleymaier K, Zitzenbacher S, Zankel A, Mayrhofer C, Sinkel C, Kueper U, Schlegel K, Ribitsch D, Guebitz GM (2016) An esterase from anaerobic Clostridium hathewayi can hydrolyze aliphatic–aromatic polyesters. Environ Sci Technol 50:2899–2907. https://doi.org/10.1021/acs.est.5b04346
Pham TH, Webb JS, Rehm BHA (2004) The role of polyhydroxyalkanoate biosynthesis by Pseudomonas aeruginosa in rhamnolipid and alginate production as well as stress tolerance and biofilm formation. Microbiology 150:3405–3413. https://doi.org/10.1099/mic.0.27357-0
Rabe M, Verdes D, Seeger S (2011) Understanding protein adsorption phenomena at solid surfaces. Adv Colloid Interf Sci 162:87–106. https://doi.org/10.1016/J.CIS.2010.12.007
Ribitsch D, Herrero Acero E, Greimel K, Dellacher A, Zitzenbacher S, Marold A, Rodriguez RD, Steinkellner G, Gruber K, Schwab H, Guebitz GM (2012) A new esterase from Thermobifida halotolerans hydrolyses polyethylene terephthalate (PET) and polylactic acid (PLA). Polymers (Basel) 4:617–629. https://doi.org/10.3390/polym4010617
Ribitsch D, Yebra AO, Zitzenbacher S, Wu J, Nowitsch S, Steinkellner G, Greimel K, Doliska A, Oberdorfer G, Gruber CC, Gruber K, Schwab H, Stana-Kleinschek K, Acero EH, Guebitz GM (2013) Fusion of binding domains to Thermobifida cellulosilytica cutinase to tune sorption characteristics and enhancing PET hydrolysis. Biomacromolecules 14:1769–1776. https://doi.org/10.1021/bm400140u
Ribitsch D, Herrero Acero E, Przylucka A, Zitzenbacher S, Marold A, Gamerith C, Tscheließnig R, Jungbauer A, Rennhofer H, Lichtenegger H, Amenitsch H, Bonazza K, Kubicek CP, Druzhinina IS, Guebitz GM (2015) Enhanced cutinase-catalyzed hydrolysis of polyethylene terephthalate by covalent fusion to hydrophobins. Appl Environ Microbiol 81:3586–3592. https://doi.org/10.1128/AEM.04111-14
Ribitsch D, Hromic A, Zitzenbacher S, Zartl B, Gamerith C, Pellis A, Jungbauer A, Łyskowski A, Steinkellner G, Gruber K, Tscheliessnig R, Herrero Acero E, Guebitz GM (2017) Small cause, large effect: structural characterization of cutinases from Thermobifida cellulosilytica. Biotechnol Bioeng 114:2481–2488. https://doi.org/10.1002/bit.26372
Ronkvist ÅM, Xie W, Lu W, Gross RA (2009) Cutinase-catalyzed hydrolysis of poly(ethylene terephthalate). Macromolecules 42:5128–5138. https://doi.org/10.1021/ma9005318
Sen S, Puskas J (2015) Green polymer chemistry: enzyme catalysis for polymer functionalization. Molecules 20:9358–9379. https://doi.org/10.3390/molecules20059358
Shirke AN, Basore D, Butterfoss GL, Bonneau R, Bystroff C, Gross RA (2016) Toward rational thermostabilization of Aspergillus oryzae cutinase: insights into catalytic and structural stability. Proteins Struct Funct Bioinf 84:60–72. https://doi.org/10.1002/prot.24955
Silva C, Da S, Silva N, Matamá T, Araújo R, Martins M, Chen SJ, Wu J, Casal M, Cavaco-Paulo A (2011) Engineered Thermobifida fusca cutinase with increased activity on polyester substrates. Biotechnol J 6:1230–1239. https://doi.org/10.1002/biot.201000391
Silva CM, Carneiro F, O'neill A, Fonseca LP, Cabral JSM, Gübitz GM, Cavaco-Paulo A (2005) Cutinase – a new tool for biomodification of synthetic fibers. J Polym Sci A Polym Chem 43(11):2448–2450
Sinsereekul N, Wangkam T, Thamchaipenet A, Srikhirin T, Eurwilaichitr L, Champreda V (2010) Recombinant expression of BTA hydrolase in Streptomyces rimosus and catalytic analysis on polyesters by surface plasmon resonance. Appl Microbiol Biotechnol 86(6):1775–1784. https://doi.org/10.1007/s00253-010-2465-y
Smith JK, Hounshell DA (1985) Wallace H. Carothers and fundamental research at Du Pont. Science (80-) 229:436–442. https://doi.org/10.1126/science.229.4712.436
Takahashi T, Maeda H, Yoneda S, Ohtaki S, Yamagata Y, Hasegawa F, Gomi K, Nakajima T, Abe K (2005) The fungal hydrophobin RolA recruits polyesterase and laterally moves on hydrophobic surfaces. Mol Microbiol 57:1780–1796. https://doi.org/10.1111/j.1365-2958.2005.04803.x
Then J, Wei R, Oeser T, Gerdts A, Schmidt J, Barth M, Zimmermann W (2016) A disulfide bridge in the calcium binding site of a polyester hydrolase increases its thermal stability and activity against polyethylene terephthalate. FEBS Open Bio 6:425–432. https://doi.org/10.1002/2211-5463.12053
Thumarat U, Nakamura R, Kawabata T, Suzuki H, Kawai F (2012) Biochemical and genetic analysis of a cutinase-type polyesterase from a thermophilic Thermobifida alba AHK119. Appl Microbiol Biotechnol 95:419–430. https://doi.org/10.1007/s00253-011-3781-6
Verger R (1997) “Interfacial activation” of lipases: facts and artifacts. Trends Biotechnol 15:32–38. https://doi.org/10.1016/S0167-7799(96)10064-0
Wei R, Oeser T, Schmidt J, Meier R, Barth M, Then J, Zimmermann W (2016) Engineered bacterial polyester hydrolases efficiently degrade polyethylene terephthalate due to relieved product inhibition. Biotechnol Bioeng 113:1658–1665. https://doi.org/10.1002/bit.25941
Wei R, Oeser T, Then J, Kühn N, Barth M, Schmidt J, Zimmermann W (2014) Functional characterization and structural modeling of synthetic polyester-degrading hydrolases from Thermomonospora curvata. AMB Express 4:44. https://doi.org/10.1186/s13568-014-0044-9
Wessels J, De Vries O, Asgeirsdottir SA, Schuren F (1991) Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3:793–799. https://doi.org/10.1105/tpc.3.8.793
Whiteford JR, Spanu PD (2002) Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol 3:391–400. https://doi.org/10.1046/j.1364-3703.2002.00129.x
Wills C (2007) Principles of population genetics, 4th edition. J Hered 98:382–382. https://doi.org/10.1093/jhered/esm035
Yoshida S, Hiraga K, Takehana T, Taniguchi I, Yamaji H, Maeda Y, Toyohara K, Miyamoto K, Kimura Y, Oda K (2016) A bacterium that degrades and assimilates poly(ethylene terephthalate). Science (80-) 351:1196–1199. https://doi.org/10.1126/science.aad6359
Zimmermann W, Billig S (2010) Enzymes for the biofunctionalization of poly(ethylene terephthalate). Springer, Heidelberg, pp 97–120
Zumstein MT, Rechsteiner D, Roduner N, Perz V, Ribitsch D, Guebitz GM, Kohler H-PE, McNeill K, Sander M (2017) Enzymatic hydrolysis of polyester thin films at the nanoscale: effects of polyester structure and enzyme active-site accessibility. Environ Sci Technol 51:7476–7485. https://doi.org/10.1021/acs.est.7b01330
Acknowledgements
This review was supported by the Federal Ministry of Science, Research and Economy (BMWFW), the Federal Ministry of Traffic, Innovation and Technology (bmvit), the Styrian Business Promotion Agency (SFG), the Standortagentur Tirol, the Government of Lower Austria, and ZIT - Technology Agency of the City of Vienna through the COMET-Funding Program managed by the Austrian Research Promotion Agency FFG.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Biundo, A., Ribitsch, D. & Guebitz, G.M. Surface engineering of polyester-degrading enzymes to improve efficiency and tune specificity. Appl Microbiol Biotechnol 102, 3551–3559 (2018). https://doi.org/10.1007/s00253-018-8850-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-8850-7