Xylonolactonase from Caulobacter crescentus Is a Mononuclear Nonheme Iron Hydrolase

Johan Pääkkönen, Leena Penttinen, Martina Andberg, Anu Koivula, Nina Hakulinen, Juha Rouvinen, Janne Jänis*

*Corresponding author for this work

Research output: Contribution to journalArticleScientificpeer-review

7 Citations (Scopus)

Abstract

Caulobacter crescentus xylonolactonase (Cc XylC, EC 3.1.1.68) catalyzes an intramolecular ester bond hydrolysis over a nonenzymatic acid/base catalysis. Cc XylC is a member of the SMP30 protein family, whose members have previously been reported to be active in the presence of bivalent metal ions, such as Ca2+, Zn2+, and Mg2+. By native mass spectrometry, we studied the binding of several bivalent metal ions to Cc XylC and observed that it binds only one of them, namely, the Fe2+ cation, specifically and with a high affinity (Kd = 0.5 μM), pointing out that Cc XylC is a mononuclear iron protein. We propose that bivalent metal cations also promote the reaction nonenzymatically by stabilizing a short-lived bicyclic intermediate on the lactone isomerization reaction. An analysis of the reaction kinetics showed that Cc XylC complexed with Fe2+ can speed up the hydrolysis of d-xylono-1,4-lactone by 100-fold and that of d-glucono-1,5-lactone by 10-fold as compared to the nonenzymatic reaction. To our knowledge, this is the first discovery of a nonheme mononuclear iron-binding enzyme that catalyzes an ester bond hydrolysis reaction.

Original languageEnglish
Pages (from-to)3046-3049
JournalBiochemistry
Volume60
Issue number41
DOIs
Publication statusPublished - 19 Oct 2021
MoE publication typeA1 Journal article-refereed

Funding

This work received support from the Academy of Finland through the SA-ENGBIOCAT (Grant Nos. 287241 and 288677) and PENTOX (Grant No. 322610) projects. The FT-ICR facility is supported by Biocenter Finland (FINStruct), Biocenter Kuopio, the European Regional Development Fund (Grant No. A70135), and the European Union’s Horizon 2020 Research and Innovation Programme (EU FT-ICR MS project; Grant No. 731077).

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