A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold

Microbial carboxylesterases are important biocatalysts that selectively hydrolyze an extensive range of esters. Here, we report the biochemical and structural characterization of an atypical carboxylesterase from Bacillus coagulans (BCE), endowed with high enantioselectivity toward different 1,2-O-i...

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Main Authors: De Vitis, Valerio, Nakhnoukh, Cristina, Pinto, Andrea, Contente, Martina L., Barbiroli, Alberto, Milani, Mario, Bolognesi, Martino, Molinari, Francesco, Gourlay, Louise J., Romano, Diego
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Published: Wiley 2018
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Online Access:https://eprints.nottingham.ac.uk/49818/
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author De Vitis, Valerio
Nakhnoukh, Cristina
Pinto, Andrea
Contente, Martina L.
Barbiroli, Alberto
Milani, Mario
Bolognesi, Martino
Molinari, Francesco
Gourlay, Louise J.
Romano, Diego
author_facet De Vitis, Valerio
Nakhnoukh, Cristina
Pinto, Andrea
Contente, Martina L.
Barbiroli, Alberto
Milani, Mario
Bolognesi, Martino
Molinari, Francesco
Gourlay, Louise J.
Romano, Diego
author_sort De Vitis, Valerio
building Nottingham Research Data Repository
collection Online Access
description Microbial carboxylesterases are important biocatalysts that selectively hydrolyze an extensive range of esters. Here, we report the biochemical and structural characterization of an atypical carboxylesterase from Bacillus coagulans (BCE), endowed with high enantioselectivity toward different 1,2-O-isopropylideneglycerol (IPG or solketal) esters. BCE efficiently catalyzes the production of enantiopure (S)-IPG, a chiral building block for the synthesis of β-blockers, glycerophospholipids, and prostaglandins; efficient hydrolysis was observed up to 65 °C. To gain insight into the mechanistic bases of such enantioselectivity, we solved the crystal structures of BCE in apo- and glycerol-bound forms at resolutions of 1.9 and 1.8 Å, respectively. In silico docking studies on the BCE structure confirmed that IPG esters with small acyl chains (≤ C6) were easily accommodated in the active site pocket, indicating that small conformational changes are necessary to accept longer substrates. Furthermore, docking studies suggested that enantioselectivity may be due to an improved stabilization of the tetrahedral reaction intermediate for the S-enantiomer. Contrary to the above functional data implying nonlipolytic functions, BCE displays a lipase-like 3D structure that hosts a “lid” domain capping the main entrance to the active site. In lipases the lid mediates catalysis through interfacial activation, a process that we did not observe for BCE. Overall, we present the functional-structural properties of an atypical carboxyl esterase that has nonlipase-like functions, yet possesses a lipase-like 3D fold. Our data provide original enzymatic information in view of BCE applications as an inexpensive, efficient biocatalyst for the production of enantiopure (S)-IPG.
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spelling nottingham-498182020-05-04T19:26:14Z https://eprints.nottingham.ac.uk/49818/ A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold De Vitis, Valerio Nakhnoukh, Cristina Pinto, Andrea Contente, Martina L. Barbiroli, Alberto Milani, Mario Bolognesi, Martino Molinari, Francesco Gourlay, Louise J. Romano, Diego Microbial carboxylesterases are important biocatalysts that selectively hydrolyze an extensive range of esters. Here, we report the biochemical and structural characterization of an atypical carboxylesterase from Bacillus coagulans (BCE), endowed with high enantioselectivity toward different 1,2-O-isopropylideneglycerol (IPG or solketal) esters. BCE efficiently catalyzes the production of enantiopure (S)-IPG, a chiral building block for the synthesis of β-blockers, glycerophospholipids, and prostaglandins; efficient hydrolysis was observed up to 65 °C. To gain insight into the mechanistic bases of such enantioselectivity, we solved the crystal structures of BCE in apo- and glycerol-bound forms at resolutions of 1.9 and 1.8 Å, respectively. In silico docking studies on the BCE structure confirmed that IPG esters with small acyl chains (≤ C6) were easily accommodated in the active site pocket, indicating that small conformational changes are necessary to accept longer substrates. Furthermore, docking studies suggested that enantioselectivity may be due to an improved stabilization of the tetrahedral reaction intermediate for the S-enantiomer. Contrary to the above functional data implying nonlipolytic functions, BCE displays a lipase-like 3D structure that hosts a “lid” domain capping the main entrance to the active site. In lipases the lid mediates catalysis through interfacial activation, a process that we did not observe for BCE. Overall, we present the functional-structural properties of an atypical carboxyl esterase that has nonlipase-like functions, yet possesses a lipase-like 3D fold. Our data provide original enzymatic information in view of BCE applications as an inexpensive, efficient biocatalyst for the production of enantiopure (S)-IPG. Wiley 2018-01-11 Article PeerReviewed De Vitis, Valerio, Nakhnoukh, Cristina, Pinto, Andrea, Contente, Martina L., Barbiroli, Alberto, Milani, Mario, Bolognesi, Martino, Molinari, Francesco, Gourlay, Louise J. and Romano, Diego (2018) A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold. FEBS Journal . ISSN 1742-4658 carboxylesterase; IPG; Bacillus coagulans; crystal structure; lipase enantioselective. http://onlinelibrary.wiley.com/doi/10.1111/febs.14368/abstract doi:10.1111/febs.14368 doi:10.1111/febs.14368
spellingShingle carboxylesterase; IPG; Bacillus coagulans; crystal structure; lipase
enantioselective.
De Vitis, Valerio
Nakhnoukh, Cristina
Pinto, Andrea
Contente, Martina L.
Barbiroli, Alberto
Milani, Mario
Bolognesi, Martino
Molinari, Francesco
Gourlay, Louise J.
Romano, Diego
A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold
title A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold
title_full A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold
title_fullStr A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold
title_full_unstemmed A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold
title_short A stereospecific carboxyl esterase from Bacillus coagulans hosting nonlipase activity within a lipase-like fold
title_sort stereospecific carboxyl esterase from bacillus coagulans hosting nonlipase activity within a lipase-like fold
topic carboxylesterase; IPG; Bacillus coagulans; crystal structure; lipase
enantioselective.
url https://eprints.nottingham.ac.uk/49818/
https://eprints.nottingham.ac.uk/49818/
https://eprints.nottingham.ac.uk/49818/