BIOCHEMICAL
Vol. 75, No. 3, 1977
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
ATOMIC COORDINATES FOR THE CHLOROPHYLL CORE OF A BACTERIOCHLOROPHYLL &-PROTEIN
FROM
GREEN PHOTOSYNTHETIC BACTERIA R. E. Fenna,*
L. F. Ten Eyck,
and B. W. Matthews
Institute of Molecular Biology and Department of Physics University of Oregon, Eugene, Oregon 97403, U.S.A.
Received
February
23,1977
Summary: Preliminary atomic coordinates are presented for the seven bacteriochlorophylls constituting the core of one subunit of the trimeric water soluble bacteriochlorophyll a-protein from the green photosynthetic bacterium Prosthecochloris aestuarii, arain 2K, formerly identified as limicola, strain 2K. The coordinates were derived from a 2.8 i%%EO, electron density map based on four isomorphous heavy-atom derivatives, and adjusted to have stereochemically acceptable bond lengths and angles. The three-dimensional protein
from
a green
crystallography limicola, (Ref.
strain
centers of seven
bacterium,
communication which
antenna (3),
[The
pigment
consists
of three
structure isomorphous
heavy-atom
with
greater
certainty
not
possible
at this
However,
the electron
chlorophyll
core
coordinates
for
quite this
chlorophyll
identical
has been
density clearly, part
inclusion
the
coordinates
map does show the and permits
us to present
the
(Fig.
1).
initial
to be defined acid
the whole
general
of a core
of a fourth
structure
for
from
reaction
of protein
map used for
by the
permitting
to present
photochemical
an envelope
density
The energy
each consisting
In the absence of the amino
(4). time
to the
within
improved
derivative,
aestuarii
of excitation
subunits,
of the electron
determination
Chlorobium
as Prosthecochloris
in the transfer
enclosed
the quality
designated
by X-ray
J. M. Olson and N. Pfennig).]
from
chlorobium
&-containing
has been determined
previously
mediates
bacteriochlorophylls
Recently
bacterium
2K, has now been identified
2 and personal
bulk
of a bacteriochlorophyll
photosynthetic
(1).
chlorophyll-protein, the
structure
sequence,
it
is
molecule.
arrangement
of the
preliminary
of the molecule.
*Present address: Molecular Biology Los Angeles, Los Angeles, California Copyright 0 I977 by Academic Press, Inc. AU rights of reproduction in any form reserved.
Institute, 90024.
University
of California
at
751 ISSN
0006291
X
Vol. 75, No. 3, 1977
Figure
1.
BIOCHEMICAL
Schematic diagram showing one subunit of the bacteriochlorophyllprotein. For clarity, the magnesium atoms, chlorophyll ring substituents and phytyl chains, except for the first bond, have been omitted. The direction of view is from the three-fold axis, which is horizontal, towards the exterior of the molecule.
The coordinates in a Richards electron
the
ethyl ring
map (2.8
geometry
was first were
substituents saturated Markers
obtained
(5,6).
8) does
of the model
aligned
possible,
with
The "raw" rotating
(Rms deviations
not permit
to coincide
as far
single
and the phytyl
chains.
Buckling
then
placed
both
a (Fig.
in the
the model
coordinates,
electron
and translating
that
were
part
a so as to minimize atoms, ranged
i.e., from
not
of
porphyrin
map, and then to place in Ring
in ethyl
the
II
ring
which
is
chlorophyllide
map to agree,
as well
a. as
density. then
of ethyl
checked
Cl-C6,
C9-C.22,
C27-C30,
0.14
1 to 0.17
fi for
and idealized
chlorophyllide
the rms deviation
752
of each
in order
was allowed
and the electron
individual on that
density
bonds
density
so obtained,
of
portion
2) but
of the
as possible,
the electron
the various
of the core
the resolution
conjugated
with
model
visualization
made about
bacteriochlorophyll corresponding
Because
The rigid
a (7).
a skeletal
was based,
in bacteriochlorophyll were
by building
comparator
chlorophyllide
rotations
first
were
optical
density
atoms,
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
a cormion to
between
the
C32, C33, Nl-N4, the
by
seven chlorophylls.)
and 01.
BIOCHEMICAL
Vol. 75, No. 3, 1977
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
CH3 34
Figure
2.
The structure used in Table
The coordinates squares
of all
procedure
same time
the
raw coordinates were
for
of a thousand
rotated
ethyl
of the
Handbook
of Chemistry
equidistant
from toward
The idealized in Table
I,
used for
ethyl
Crystals
where
its
times
(10).
nitrogen fifth
coordinates
for
the numbering
chlorophyllide crystallographic of the chlorophyll
constraints,
bond length
as adherence
to
and angle
to the raw
of the chlorin
ring
to coincide
described
above.
and angles
and at
as desired
the atoms
where
with
the
The "standard"
were
Each magnesium
ligands,
the apparent
by a least
as closely the
portion
bond lengths
and Physics four
to fit
the atom numbering
adjusted
and angle
as heavily
coordinates
substituent
then
application
used to force
chlorophyllide
dimensions
model
the conjugated were
were
bond length
idealized
ten
2 showing
atoms
In this
weighted
weights
the orthogonal
the (8,9).
except
plane
enforces
requires
coordinates,
ring
the remaining
which
the
constraints
of bacteriochlorophyll I.
taken
from
the
atom was located
and displaced
0.4 8, from
the
ligand. the
seven
scheme, a (7).
shown
bacteriochlorophylls in Figure
The coordinates
axes a*,
b, and c.
protein
have space
753
are
2, is are
group
based
on that
in Angstroms
P63 with
given
cell
along
Vol. 75, No. 3, 1977
BIOCt ?EMICAL AND BIOPHYSICA
Table I “wl
I
Ld
i ri I H7
b3.b ‘1.‘ ‘,. 1 Lb.* bb..
COMM’JN!CATIONS
Vol.75,
BIOCHEMICAL
No. 3, 1977
dimensions
a = b = 112.4
fractional
crystallographic
coordinates
(X,Y,Z)
in Table the
0.3
X,
phytyl tions
0.01027
X
Y
=
0.00890
Y
Z
=
0.01016
Z
relating
I by 120"
the
and unlikely chains,
giving
in terms
about
the
of the orthogonal
average
to exceed
the
errors
of some of these
and passes
axis contained
the conjugated error
could groups
will
are
through
within
the coordinates
a complete
portions
as large,
the point
of the coordinates
generate
For the ring
be twice
bacteriochlorophyll-
Rotations
in the coordinates
0.5 i.
X
of the
y = l/3).
this
molecules within
0.00514
the subunits
x = 2/3,
and 240"
that
+
to the Z axis
1, Y = 0 1 (i.e.,
molecule
(x,y,z)
=
21 bacteriochlorophyll
phyll
The transformation
x
is parallel
We estimate
8.
coordinates
axis
molecule
X = 64.89
1, c = 98.4
is as follows:
The three-fold protein
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
of
trimer.
of each bacteriochloroquoted
in Table
substituents,
I is about
including
and the detailed
conforma-
uncertain.
Ackno;laedgmehnt;: We are particularly grateful to Dr. John M. Olson for prove ing t e acteriochlorophyll &-protein , and thank Dr. W. R. Kester for This study was supported in part the use of his "Rotate" computer program. by grants from the National Science Foundation (BMS 74-18407) and the National Institutes of Health (GM 15423), and by a Public Health Service Career Development Award to B.W.M. (GM 70585) from the Institutes of General Medical Science.
REFERENCES 1.
Fenna,
R. E.,
and Matthews,
2.
Pfennig,
N.,
3.
Olson, J. M. (1966) In "The eds., pp. 413-425, Academic
4.
Fenna, R. E., 28, in press.
and Biebl,
B. W. (1975)
H. (1976)
and Matthews,
Arch.
Nature
258,
Microbial.
573-577. 110,
Chlorophylls", L. P. Vernon Press, New York. B. W. (1977)
755
Brookhaven
3-12. and G. R. Seely,
Symposium
in Biology
the
BIOCHEMICAL
Vol. 75, No. 3, 1977
5. 6.
Richards, Colman,
F. M. (1968) P. M.,
J. Mol.
Jansonius,
AND BIOPHYSICAL
Biol.
37,
RESEARCH COMMUNICATIONS
225-230.
J. N., and Matthews,
J. Mol.
B. W. (1972)
Biol.
70, 701-724. 7.
Chow,
H-C.,
Serlin,
R. S.,
and Strouse,
C. E. (1975)
J. Amer.
Chem. Sot.
97, 7230-7237. 8.
Ten Eyck, Crystallogr.
9.
Oodson, E. J., A3& 311-315.
10.
L. F., Weaver, L. H., A32-, 349-350.
and Matthews,
Isaacs, N. W., and Rollett,
CRC Handbook of Chemistry Rubber Co. 52, F-173.
and Physics
756
(1971)
B. W. (1976)
J. S. (1976) R. C. Weast,
Acta
Acta ed.,
Crystallogr. Chemical
Vol. 75, No. 3, 1977
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
ATOMIC COORDINATES FOR THE CHLOROPHYLL CORE OF A BACTERIOCHLOROPHYLL &-PROTEIN
FROM
GREEN PHOTOSYNTHETIC BACTERIA R. E. Fenna,*
L. F. Ten Eyck,
and B. W. Matthews
Institute of Molecular Biology and Department of Physics University of Oregon, Eugene, Oregon 97403, U.S.A.
Received
February
23,1977
Summary: Preliminary atomic coordinates are presented for the seven bacteriochlorophylls constituting the core of one subunit of the trimeric water soluble bacteriochlorophyll a-protein from the green photosynthetic bacterium Prosthecochloris aestuarii, arain 2K, formerly identified as limicola, strain 2K. The coordinates were derived from a 2.8 i%%EO, electron density map based on four isomorphous heavy-atom derivatives, and adjusted to have stereochemically acceptable bond lengths and angles. The three-dimensional protein
from
a green
crystallography limicola, (Ref.
strain
centers of seven
bacterium,
communication which
antenna (3),
[The
pigment
consists
of three
structure isomorphous
heavy-atom
with
greater
certainty
not
possible
at this
However,
the electron
chlorophyll
core
coordinates
for
quite this
chlorophyll
identical
has been
density clearly, part
inclusion
the
coordinates
map does show the and permits
us to present
the
(Fig.
1).
initial
to be defined acid
the whole
general
of a core
of a fourth
structure
for
from
reaction
of protein
map used for
by the
permitting
to present
photochemical
an envelope
density
The energy
each consisting
In the absence of the amino
(4). time
to the
within
improved
derivative,
aestuarii
of excitation
subunits,
of the electron
determination
Chlorobium
as Prosthecochloris
in the transfer
enclosed
the quality
designated
by X-ray
J. M. Olson and N. Pfennig).]
from
chlorobium
&-containing
has been determined
previously
mediates
bacteriochlorophylls
Recently
bacterium
2K, has now been identified
2 and personal
bulk
of a bacteriochlorophyll
photosynthetic
(1).
chlorophyll-protein, the
structure
sequence,
it
is
molecule.
arrangement
of the
preliminary
of the molecule.
*Present address: Molecular Biology Los Angeles, Los Angeles, California Copyright 0 I977 by Academic Press, Inc. AU rights of reproduction in any form reserved.
Institute, 90024.
University
of California
at
751 ISSN
0006291
X
Vol. 75, No. 3, 1977
Figure
1.
BIOCHEMICAL
Schematic diagram showing one subunit of the bacteriochlorophyllprotein. For clarity, the magnesium atoms, chlorophyll ring substituents and phytyl chains, except for the first bond, have been omitted. The direction of view is from the three-fold axis, which is horizontal, towards the exterior of the molecule.
The coordinates in a Richards electron
the
ethyl ring
map (2.8
geometry
was first were
substituents saturated Markers
obtained
(5,6).
8) does
of the model
aligned
possible,
with
The "raw" rotating
(Rms deviations
not permit
to coincide
as far
single
and the phytyl
chains.
Buckling
then
placed
both
a (Fig.
in the
the model
coordinates,
electron
and translating
that
were
part
a so as to minimize atoms, ranged
i.e., from
not
of
porphyrin
map, and then to place in Ring
in ethyl
the
II
ring
which
is
chlorophyllide
map to agree,
as well
a. as
density. then
of ethyl
checked
Cl-C6,
C9-C.22,
C27-C30,
0.14
1 to 0.17
fi for
and idealized
chlorophyllide
the rms deviation
752
of each
in order
was allowed
and the electron
individual on that
density
bonds
density
so obtained,
of
portion
2) but
of the
as possible,
the electron
the various
of the core
the resolution
conjugated
with
model
visualization
made about
bacteriochlorophyll corresponding
Because
The rigid
a (7).
a skeletal
was based,
in bacteriochlorophyll were
by building
comparator
chlorophyllide
rotations
first
were
optical
density
atoms,
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
a cormion to
between
the
C32, C33, Nl-N4, the
by
seven chlorophylls.)
and 01.
BIOCHEMICAL
Vol. 75, No. 3, 1977
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
CH3 34
Figure
2.
The structure used in Table
The coordinates squares
of all
procedure
same time
the
raw coordinates were
for
of a thousand
rotated
ethyl
of the
Handbook
of Chemistry
equidistant
from toward
The idealized in Table
I,
used for
ethyl
Crystals
where
its
times
(10).
nitrogen fifth
coordinates
for
the numbering
chlorophyllide crystallographic of the chlorophyll
constraints,
bond length
as adherence
to
and angle
to the raw
of the chlorin
ring
to coincide
described
above.
and angles
and at
as desired
the atoms
where
with
the
The "standard"
were
Each magnesium
ligands,
the apparent
by a least
as closely the
portion
bond lengths
and Physics four
to fit
the atom numbering
adjusted
and angle
as heavily
coordinates
substituent
then
application
used to force
chlorophyllide
dimensions
model
the conjugated were
were
bond length
idealized
ten
2 showing
atoms
In this
weighted
weights
the orthogonal
the (8,9).
except
plane
enforces
requires
coordinates,
ring
the remaining
which
the
constraints
of bacteriochlorophyll I.
taken
from
the
atom was located
and displaced
0.4 8, from
the
ligand. the
seven
scheme, a (7).
shown
bacteriochlorophylls in Figure
The coordinates
axes a*,
b, and c.
protein
have space
753
are
2, is are
group
based
on that
in Angstroms
P63 with
given
cell
along
Vol. 75, No. 3, 1977
BIOCt ?EMICAL AND BIOPHYSICA
Table I “wl
I
Ld
i ri I H7
b3.b ‘1.‘ ‘,. 1 Lb.* bb..
COMM’JN!CATIONS
Vol.75,
BIOCHEMICAL
No. 3, 1977
dimensions
a = b = 112.4
fractional
crystallographic
coordinates
(X,Y,Z)
in Table the
0.3
X,
phytyl tions
0.01027
X
Y
=
0.00890
Y
Z
=
0.01016
Z
relating
I by 120"
the
and unlikely chains,
giving
in terms
about
the
of the orthogonal
average
to exceed
the
errors
of some of these
and passes
axis contained
the conjugated error
could groups
will
are
through
within
the coordinates
a complete
portions
as large,
the point
of the coordinates
generate
For the ring
be twice
bacteriochlorophyll-
Rotations
in the coordinates
0.5 i.
X
of the
y = l/3).
this
molecules within
0.00514
the subunits
x = 2/3,
and 240"
that
+
to the Z axis
1, Y = 0 1 (i.e.,
molecule
(x,y,z)
=
21 bacteriochlorophyll
phyll
The transformation
x
is parallel
We estimate
8.
coordinates
axis
molecule
X = 64.89
1, c = 98.4
is as follows:
The three-fold protein
AND BIOPHYSICAL RESEARCH COMMUNICATIONS
of
trimer.
of each bacteriochloroquoted
in Table
substituents,
I is about
including
and the detailed
conforma-
uncertain.
Ackno;laedgmehnt;: We are particularly grateful to Dr. John M. Olson for prove ing t e acteriochlorophyll &-protein , and thank Dr. W. R. Kester for This study was supported in part the use of his "Rotate" computer program. by grants from the National Science Foundation (BMS 74-18407) and the National Institutes of Health (GM 15423), and by a Public Health Service Career Development Award to B.W.M. (GM 70585) from the Institutes of General Medical Science.
REFERENCES 1.
Fenna,
R. E.,
and Matthews,
2.
Pfennig,
N.,
3.
Olson, J. M. (1966) In "The eds., pp. 413-425, Academic
4.
Fenna, R. E., 28, in press.
and Biebl,
B. W. (1975)
H. (1976)
and Matthews,
Arch.
Nature
258,
Microbial.
573-577. 110,
Chlorophylls", L. P. Vernon Press, New York. B. W. (1977)
755
Brookhaven
3-12. and G. R. Seely,
Symposium
in Biology
the
BIOCHEMICAL
Vol. 75, No. 3, 1977
5. 6.
Richards, Colman,
F. M. (1968) P. M.,
J. Mol.
Jansonius,
AND BIOPHYSICAL
Biol.
37,
RESEARCH COMMUNICATIONS
225-230.
J. N., and Matthews,
J. Mol.
B. W. (1972)
Biol.
70, 701-724. 7.
Chow,
H-C.,
Serlin,
R. S.,
and Strouse,
C. E. (1975)
J. Amer.
Chem. Sot.
97, 7230-7237. 8.
Ten Eyck, Crystallogr.
9.
Oodson, E. J., A3& 311-315.
10.
L. F., Weaver, L. H., A32-, 349-350.
and Matthews,
Isaacs, N. W., and Rollett,
CRC Handbook of Chemistry Rubber Co. 52, F-173.
and Physics
756
(1971)
B. W. (1976)
J. S. (1976) R. C. Weast,
Acta
Acta ed.,
Crystallogr. Chemical
