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ELSEVIER Biochimica et Biophysica Acta 1188 (1994) 260-270
BB
Biochi~ic~a
etBiophysica A~ta
Binding of carboxylate anions at the non-heme Fe(II) of PS II.
I. Effects on the QAFe 2÷ and QAFe 3+ EPR spectra
and the redox properties
of the iron
Y. Deligiannakis a V. Petrouleas a,* B.A. Diner b
a Institute of Materials Science, NCSR Democritos, 15310 Aghia Paraskeui A ttiki, Athens, Greece
b Central Research and Development Department, Experimental Station, E.I. DuPont de Nemours Co., Wilmington, DE 19880-0173, USA
Received 10 December 1993; revised 7 July 1994
Abstract
We have examined the effects of a number of carboxylate anions on the iron-quinone complex of Photosystem II (PS II).
Typical effects are the following. In the state QAFe 2+ oxalate enhances significantly the g = 1.84 EPR resonance while, for
example, glycolate and glyoxylate suppress it. The anions have variable effects on the iron midpoint potential. Formate and
oxalate raise significantly the E m of the iron. Glycolate lowers the E m significantly and the E m shows a weak pH dependence. In
the presence of glycolate the native plastosemiquinone (Q~/QBH2 couple) can oxidise the iron. Glyoxylate also lowers the Em,
but the E m shows a greater pH dependence than with glycolate but still weaker than the - 60 mV/pH unit of the untreated iron.
The Fe 3+ EPR spectra are characterised by small but distinct shifts, while in addition an unusual resonance at close to g = 4.3 is
observed. These as well as the temperature dependence of the spectra are analysed by a spin-Hamiltonian model. Comparison
with competition studies in the companion paper indicates that the anions bind as iron ligands displacing bicarbonate.
Keywords: Photosystem II; Iron-quinone complex; EPR; Carboxylate anion
1. Introduction
The non-heme iron of Photosystem II (PS II) has a
number of properties which differentiate it from its
analogue in the purple-photosynthetic bacteria. Be-
sides spectroscopic differences and its redox activity
the iron of PS II can reversibly bind small molecules
such as NO [1] or CN [2]. Bicarbonate-NO competition
studies have suggested that bicarbonate is the natural
labile ligand to the non-heme iron [3]. Normal rates of
electron flow require the presence of this anion (see,
e.g., Refs. [4,5]. The mode of bicarbonate binding and
action, however, is not fully understood at present.
Abbreviations: PS II, Photosystem II; BBY, thylakoid membrane
fragments isolated according to Refs. [10-12]; QA, primary quinone
electron acceptor; QB, secondary quinone electron acceptor; Mes,
4-morpholinethanesulfonic acid; Hepes, 4-(2-hydroxyethyl)-l-
piperazineethanesulfonic acid; Tris, tris(hydroxymethyl)amino-
methane.
* Corresponding author. Fax: + 30 1 6519430.
0005-2728/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved
SSDI 0005-2728(94)00132-4
A well known class of proteins which require CO 2
for their functioning are the transferrins. In the trans-
ferrin proteins CO 2 in the form of carbonate is re-
quired as a synergistic anion for iron binding. An X-ray
structure determination of lactoferrin has shown that
the protein provides four ligands to the iron (two
tyrosines one histidine and one aspartate) while car-
bonate is bound to the iron as a bidentate ligand [6].
Schlabach and Bates [7] have examined an extensive
list of carboxylate anions which can substitute for car-
bonate as the synergistic anion in Fe-transferrin. More
recently Dubach et al. [8] have reported on EPR spec-
tra of iron-transferrin anion complexes and have pro-
vided insights into the mode of binding of these anions
as well as of carbonate to the iron.
Prompted by these studies, we examined in a prelim-
inary report [9] the effect of these anions upon their
substitution of bicarbonate in Photosystem II. We elab-
orate here on the effects of these anions on the QAFe 2+
and QAFe 3+ EPR spectra and the redox properties of
the Fe3+/Fe 2+ couple.