244 Biochbnica et Biophysica Acta, 1101 (1992) 244-248
© 1992 Elsevier Science Publishers B.V. All rights reserved 0005-2728/92/$05.00
BBABIO 43660
Cooperative transient trapping of protons by structurally
distorted chloroplast ATPase: Evidence for the proton well?
Cord Griwatz J and Wolfgang Junge
Biophysik, Fachbereich Biologic/Chemic, Unicersitiit Osnabriick, D-4500 Osnabriick (Germany)
(Received 14 April 1992)
Key words: ATPase; Proton; Protonmotive force; Photosynthesis; (Chloroplast)
The structure of membrane-bound ATPase, CFoCF1, was distorted by mild EDTA treatment, but without solubilization of CF I.
Distorted CFoCF l rapidly trapped protons from the lumen side without transport. Trapping required electric driving force,
showed very high cooperativity as function of pH and hysteresis as function of time. It is discussed under the concept of a 'proton
well'.
Introduction
The proton-translocating ATPase in thylakoid mem-
branes of chloroplasts, CFoCF t, belongs to the ubiqui-
tous class of F-type ATPases with bipartite structure.
The extrinsic portion, CF~, binds nucleotides and phos-
phate. When dissociated from its intrinsic membrane
counterpart, it exposes CF 0, a proton channel with
unparalleled selectivity. CF 0 discriminates protons
against other cations from pH 6 to 8 and even in the
presence of 300 mM KCI in the suspending medium.
This has been evaluated by flash spectrophotometry
[1]. In such experiments both photosystems are stimu-
lated for single turnover by a short flash of light. This
generates a transmembrane voltage (by 30-60 mV more
positive in the lumen) and a pH difference (about 0.05
units more acid in the lumen) [2]. Three observables
have been monitored, namely: (a) pH transients in the
lumen, (b) transients of the transmembrane voltage,
and (c) pH transients in the suspending medium [1,3,4].
When more than 50% of total CFI is solubilized by
treatment of thylakoids with some 100/zM EDTA, the
extent and the time-course of proton intake from the
lumen and of charge transfer across the membrane are
equal [1]. Proton binding by CF 0 and transfer across
Correspondence: W. Junge, Fachbereich 5, Universit~it Osnabriick,
Postfach 4469, D-4500 OsnabrOck, Germany.
J Present address: C. Griwatz, Institut fOr Klinische Chemic, Zen-
tralklinikum, Universit~it MOnster, D-4400 MOnster, Germany.
Abbreviations: DCCD, N',N'-dicyclohexylcarbodiimide; DCMU, 3-
(3,4-dichlorophenyl)-l,l-dimethylurea; NTA0 nitrolotriacetic acid.
the membrane dielectric appear to occur in synchrony.
The same holds for the coupled transfer of protons
during ATP synthesis through the holoenzyme, CFoCF ~
[5].
We report here on highly cooperative proton trap-
ping by CFoCF 1without concomitant transfer of charges
across the membrane. This effect is elicited by treat-
ment of thylakoids with very low concentrations of
EDTA, say 10/~M. It was first described several years
ago [6]. The experimental results of the previous work
were fully reproduced in this work. Further data led to
better understanding of the mechanism of this effect,
which is sketched in this article.
Materials and Methods
Thylakoids were prepared from spinach or pea by
standard procedures [1], except for the absence of
magnesium in the media (destacked thylakoids). The
ionic milieu in preparation and storage media was
domiriated by 10 mM NaCI. The procedure to evoke
transient trapping of protons was as follows. Concen-
trated stock (2-3 mg chlorophyll/ml) was diluted in
distilled water to yield a chlorophyll concentration of
10 /zM, the pH was adjusted to 7.5 at room tempera-
ture. EDTA was added, typically at 10 p.M (for neces-
sary variations, see below). After 2 rain, NaCI was
added at 10 mM to stop exposure to low ionic strength.
Longer incubation and higher concentration of EDTA
resulted in CF~ solubilization with the drastic increase
of the proton conductance by exposed CF 0. After
preincubation, methyl viologen (10 /zM) was added as
electron acceptor.