Engineering of access tunnel in haloalkane dehalogenase to minimise stability-function trade-off

R. Chaloupkova1, V. Liskova1, D. Bednar1, T. Prudnikova2,3, P. Rezacova4,5, T. Koudelakova1, E. Sebestova1, I. Kuta Smatanova2, J. Brezovsky1, J. Damborsky1,6

1Loschmidt Laboratories, Department of Experimental Biology and Research Centre for Toxic Compounds in the Environment, Faculty of Science, Masaryk University, Kamenice 5/A13, 625 00 Brno, Czech Republic
2Faculty of Science, University of South Bohemia in Ceske Budejovice, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic
3Institute of Nanobiology and Structural Biology, Academy of Sciences of the Czech Republic, Zamek 136, 373 33 Nove Hrady, Czech Republic
4Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Videnska 1083, 142 20 Prague 4 Prague, Czech Republic
5Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Flemingovo nam. 2, 166 10 Prague 6, Czech Republic
6International Clinical Research Center, St. Anne’s University Hospital, Pekarska 53, 656 91 Brno, Czech Republic
radka@chemi.muni.cz

Haloalkane dehalogenases (HLDs, EC 3.8.1.5) are bacterial enzymes with α/β-hydrolase fold, which catalyse hydrolytic conversion of a broad range of halogenated aliphatic hydrocarbons into three reaction products: an alcohol, a halide anion and a proton. HLDs catalyse the reactions of great environmental and biotechnological significance with potential application in bioremediation, biosensing, decontamination of warfare agents, synthesis of optically pure compounds, cellular imaging and protein tagging [1]. However, their use in these applications is limited by their low stability and activity under the harsh conditions. Recently constructed variant of haloalkane dehalogenase DhaA exhibited 4000-fold improved kinetic stability in 40 % (v/v) DMSO, enhanced thermostability by 16.4 °C, but 100-fold lower catalytic activity with 1,2-dibromoethane in pure buffer compared to the wild type enzyme. Enzyme stabilisation was achieved by introduction of four bulkier and mostly hydrophobic residues into the enzyme access tunnel. Introduced residues improved a contact with other residues of the access tunnel, enhanced packing of hydrophobic core and prevented entry of DMSO into the active-site cavity [2].

Herein presented study aimed to improve catalytic activity of the highly stable DhaA in buffer, with minimum loss of its stability. Systematic mutagenesis of two of the four originally modified tunnel residues (F176 and V172) resulted in a single point variant F176G possessing 32- and 10-times improved catalytic activity in buffer and in 40 % (v/v) DMSO, respectively. Thermostability of the mutant was lowered by 4 °C only. Moreover, the newly evolved variant exhibited enhanced activity towards 26 out of 30 tested halogenated compounds similarly to wild-type enzyme. Structural analysis and molecular dynamics revealed that newly introduced mutation F176G reopened previously closed tunnel in stable DhaA and increase the mobility of the two α-helices lining the tunnel, thus restoring the enzyme activity, while remaining tunnel mutations maintained its stability. Fine-tuning of amino acid residues lining the access tunnels thus represents generally-applicable strategy for minimisation of stability-function trade-off of enzymes with buried active sites [3].

1. T. Koudelakova, S. Bidmanova, P. Dvorak, A. Pavelka, R. Chaloupkova, Z. Prokop, J. Damborsky, Haloalkane Dehalogenases: Biotechnological Applications, Biotechnol. J., 8 (2013), 32-45.

2. T. Koudelakova, R. Chaloupkova, J. Brezovsky, Z. Prokop, E. Sebestova, M. Hesseler, M. Khabiri, M. Plevaka, D. Kulik, I. Kuta Smatanova, P. Rezacova, R. Ettrich, U. T. Bornscheuer, J.Damborsky, Engineering Enzyme Stability and Resistance to an Organic Cosolvent by Modification of Residues in the Access Tunnel, Angew. Chem. Int. Ed. Engl., 52 (2013), 1959–1963.

3. V. Liskova, D. Bednar, T. Holubeva, T. Prudnikova, P. Rezacova, T. Koudelakova, E. Sebestova, I. Kuta Smatanova, J. Brezovsky, R. Chaloupkova, J. Damborsky, Balancing the Stability-Activity Trade-off by Fine-Tuning Dehalogenase Access Tunnels, ChemCatChem 7 (2015), 648-659.