TY - JOUR
T1 - Xylonolactonase from Caulobacter crescentus Is a Mononuclear Nonheme Iron Hydrolase
AU - Pääkkönen, Johan
AU - Penttinen, Leena
AU - Andberg, Martina
AU - Koivula, Anu
AU - Hakulinen, Nina
AU - Rouvinen, Juha
AU - Jänis, Janne
N1 - Funding Information:
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). We thank A. Kiema for technical assistance (VTT).
Publisher Copyright:
© 2021 The Authors. Published by American Chemical Society.
PY - 2021/10/19
Y1 - 2021/10/19
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85117491980&partnerID=8YFLogxK
U2 - 10.1021/acs.biochem.1c00249
DO - 10.1021/acs.biochem.1c00249
M3 - Article
C2 - 34633186
AN - SCOPUS:85117491980
SN - 0006-2960
VL - 60
SP - 3046
EP - 3049
JO - Biochemistry
JF - Biochemistry
IS - 41
ER -