Structural and functional characterization of the paai thioesterase from Streptococcus pneumoniae reveals a dual specificity for phenylacetyl-CoA and medium-chain fatty Acyl-CoAs and a novel CoA-induced fit mechanism

Journal Publication ResearchOnline@JCU
Khandokar, Yogesh B.;Srivastava, Parul;Sarker, Subir;Swarbrick, Crystall M.D.;Aragao, David;Cowieson, Nathan;Forwood, Jade K.
Abstract

PaaI thioesterases are members of the TE13 thioesterase family that catalyze the hydrolysis of thioester bonds between coenzyme A and phenylacetyl-CoA. In this study we characterize the PaaI thioesterase from Streptococcus pneumoniae (SpPaaI), including structural analysis based on crystal diffraction data to 1.8-Å resolution, to reveal two double hotdog domains arranged in a back to back configuration. Consistent with the crystallography data, both size exclusion chromatography and small angle x-ray scattering data support a tetrameric arrangement of thioesterase domains in solution. Assessment of SpPaaI activity against a range of acyl-CoA substrates showed activity for both phenylacetyl-CoA and medium-chain fatty-acyl CoA substrates. Mutagenesis of putative active site residues reveals Asn37, Asp52, and Thr68 are important for catalysis, and size exclusion chromatography analysis and x-ray crystallography confirm that these mutants retain the same tertiary and quaternary structures, establishing that the reduced activity is not a result of structural perturbations. Interestingly, the structure of SpPaaI in the presence of CoA provides a structural basis for the observed substrate specificity, accommodating a 10-carbon fatty acid chain, and a large conformational change of up to 38 Å in the Nterminus, and a loop region involving Tyr38-Tyr39. This is the first time PaaI thioesterases have displayed a dual specificity for medium-chain acyl-CoAs substrates and phenylacetyl-CoA substrates, and we provide a structural basis for this specificity, highlighting a novel induced fit mechanism that is likely to be conserved within members of this enzyme family.

Journal

Journal of Biological Chemistry

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Volume

291

ISBN/ISSN

1083-351X

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Issue

4

Pages Count

11

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Publisher

Elsevier

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DOI

10.1074/jbc.M115.677484