Atypical mitochondria in the ellipsoid of the
photoreceptor cells of vertebrate retinas
Toyoko Ishikawa and Eichi Yamada
The fine structure of ellipsoids in a number of vertebrate retinas was studied in material prepared with various fixatives. Several atypical ellipsoidal mitochondria were found in ellipsoids
of certain animals. A peculiar configuration of the internal mitochondrial membranes caused by
fusion of the outer surfaces of adjacent cristae was found in the lamprey retina. Intramitochondrial glycogen granules and granular or filamentous intracristal inclusions were observed in
the toad and giant salamander, respectively. In photoreceptor cells of the gecko, carp, and
snake, the ellipsoid was particularly differentiated, containing modified mitochondria. The
possible functional significance of such differentiated ellipsoids is discussed briefly with respect
to the oil droplets.
Key words: retinal ellipsoid, mitochondria, infrastructure, electron microscopy,
glutaraldehyde, osmium tetroxide, glycogen.
been reported in many cell types, atypical
and specially modified ellipsoidal mitochondria found in certain animals seem to
be quite unique. In this paper the most
unusual types of ellipsoidal mitochondria
will be described, and their possible functional significance will be discussed briefly.
.he ellipsoid of photoreceptor cells is
located at the apical region of the inner
segment and appears to be homogeneous
in fresh material. It was first described as
a dense aggregation of elongated mitochondria by Sjostrand1 in his pioneering electron microscope study,1 and this has been
found to be the typical conformation of the
ellipsoid in vertebrate retinas.
During the course of a comparative study
on the retinal fine structure of a wide variety of vertebrates, it was noted that ellipsoidal mitochondria exhibit great variation
in structural details. Although a number of
atypical forms of mitochondria, or those
possessing various inclusion bodies, have
Materials and methods
Although a number of animal species from
cyclostomes to mammals, mostly adult, have been
used in the course of a comparative study on the
retinal fine structure in our laboratory, the observations described in this paper were restricted to
those animals which contain the most unusual
ellipsoidal mitochondria; they are: lampreys, carp,
giant salamanders, snakes, geckos, turtles, and
pigeons.
Since the electron microscopic image of mitochondria varies, depending upon the methods used
to fix and stain them, at least two kinds of fixatives with different ingredients were utilized for
the fixation of each animal retina. In general, the
retina, with or without the choroid and sclera,
from one eye of an individual animal was fixed in
one per cent osmium tetroxide, and the retina
from the other eye was fixed in 3 to 6 per cent
glutaraldehyde followed by a 2 hour fixation of
osmium. The fixatives were buffered with Millonig's
From the Department of Anatomy, Faculty of
Medicine, Kyushu University, Fukuoka, Japan.
This investigation was supported by Grant 2 RO1
NB 03614-06 from the National Institute of
Neurological Diseases and Blindness, National
Institutes of Health, United States Public Health
Service.
Manuscript submitted August 1, 1968; manuscript
accepted August 19, 1968.
302
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phosphate, s-collidine, or sodium cacodylate. All
of the fixed retinas were dehydrated in either a
graded series of ethanol or acetone, and embedded
in Epon. Ultrathin sections were cut mainly with
glass knives or a diamond knife on a Porter-Blum
microtome, stained with lead tartrate or lead
citrate, or 2 per cent aqueous solution of uranyl
acetate, or a combination of both. Some of the
material was stained for one hour in a block with
aqueous uranyl acetate before dehydration.
One micron sections of Epon-embedded tissue
were obtained, cut with the same microtome, and
stained with toluidine blue for histological examination. Periodic acid—Schiff reaction or Sudan
black B staining was also utilized in some cases.
Observations
Generally speaking, ellipsoids of vertebrate photoreceptor cells consist of a dense
aggregation of mitochondria. The shape
and size of these, however, vary considerably from one species to another, as do the
other types of cells and tissues. In addition,
unusual forms of mitochondria and specially modified ones are also found. For convenience, they will be described here divided into several groups according to the
patterns of their structural modification.
A very unusual form of internal mitochondrial membrane was encountered in
the ellipsoids of the lamprey, Entosphenus
japonicus. In this retina, two types of visual
cells, rods and cones, have been described.2
In an ordinary histologic preparation, the
ellipsoidal region of receptor cells appears
in two parallel rows.
Fig. 1 is an electron micrograph of the
lamprey retina, showing the ellipsoids of
the so-called rod photoreceptor cells. Mitochondria, having an elongated shape with
rather sparse cristae located vitreally, are
typical of ellipsoids. However, the mitochondria gradually increase in size toward
the scleral end of the ellipsoid. Such mitochondrial gradient in size is not infrequent
in the ellipsoid of lower vertebrates, particularly in cone ellipsoids, while those of
human photoreceptor cells,3 or of rod cells
in most animals, consist of a homogeneous
population of mitochondria. With the increase in mitochondrial size, cristae also
increase in number and are organized in
parallel array along the long axis of mito-
Atypical mitochondria in ellipsoid 303
chondria. In larger mitochondria with an
irregular contour, they are sometimes arranged in groups which are distributed at
random within a mitochondrion. In some
cases, cristae in lamellar patterns having
sharp angulations of the membranes present a zigzag course in the same way
described in some other tissues4 (Fig. 2).
A peculiar configuration of internal mitochondrial membranes can occur in these
parallel arrayed cristae and is shown by
arrows in Figs. 1 and 2. Closer examination
of this peculiar structure reveals that certain numbers of parallelly arrayed cristae
adhere tightly to each other and two membranes of adjacent cristae appear to fuse
into a dense membrane of approximately
110 A in thickness. Consequently, intercristal space or mitochondrial matrix disappears in this region. On the other hand, the
thickness of intracristal spaces of such
cristae diminishes by approximately half,
but the spaces never vanish completely.
Such membrane fusions were encountered
only between the internal mitochondrial
membranes, and were never observed between different mitochondria or between
an outer and inner mitochondrial membrane. Fig. 3 shows the peculiar configuration of internal mitochondrial membranes
sectioned in a plane nearly normal to the
structure and demonstrates its finer detail.
Other variations are atypical ellipsoidal
mitochondria which contain inclusion
bodies or material in the lumen of cristae.
Ordinarily intracristal space is fairly constant and is about 60 to 80 A in width. In
this group of ellipsoidal mitochondria, however, this space is dilated locally and contains either granular or amorphous materials. As previously reported, in the photoreceptor cells of the rat retina, the granular
inclusion in the lumen of cristae was identified as glycogen.5 Similar intramitochondrial
glycogen granules were also found in subsequent studies in retinal ellipsoids of toads,
Buto vulgaris japonicus (Fig. 7), the snake,
and the carp. It is noteworthy that glycogen-containing mitochondria in retinal tissue were always found in rods.
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304 hhikawa and Yamacla
An example of amorphous intracristal inclusion of mitochondria was observed in
the ellipsoid of the giant salamander retina,
in which rod cells are predominant. Fig. 4
shows a vertically sectioned rod cell of a
giant salamander, Megalobatrachus japonicus. The ellipsoid consists of closely packed,
rather uniform-sized mitochondria. A number of these intracristal spaces are dilated
in places and filled with a dense amorphous
material. It seems likely that further accumulation of this material enlarges not
only the lumen of the crista, but also the
mitochondrion itself.
Although most intracristal material appears in a very fine granular form under
high power (Fig. 5), filamentous inclusions
with a helical substructure were found in
some instances (Fig. 6). Very similar structures have been reported in astrocytic mitochondria of the rat.6
The third group of ellipsoidal mitochondria is very unique and is regarded as an
especially differentiated form of the ellip-
soid. Morphologically, we can distinguish
two types in this group, one of which was
found in the retina of snakes and the other
in carps and geckos.
In this study the retinas of two species
of snakes, Elaphe climacophora and Agkistrodon hcdys blomhofjii, were examined.
The retina of the former belongs to the
so-called pure cone type, and the latter
contains both rods and cones. In both
species there are single and double cones.
Single cones and the principal member of
the double cone are morphologically identical and both possess a specially differentiated ellipsoid, which has a barrel-shaped
body with a densely staining core, as shown
in Fig. 8. The ellipsoid of the accessory
member of the pair consists of ordinary
mitochondria. In this paper the description
will be restricted to the differentiated type
of ellipsoid.
Fig. 9 is a transverse section of a single
cone in Elaphe retina at the level of the
ellipsoid. Numerous mitochondria are
Text continued on p. 308.
Fig. 1. A nearly vertical section of inner segments of lamprey photoreceptor cells. The inner
segment is almost filled with tightly packed mitochondria. They are typically rod-shaped toward
the scleral end. In the latter, numerous mitochondrial cristae are arranged in parallel arrays.
The peculiar configuration of internal mitochondrial membranes appears as thick osmiophilic
lines in this low magnification electron micrograph (arrows). OS, outer segment; B, basal body.
Fixed in Osd-Millonig's buffer, stained with lead tartrate. (Original magnification x8,000.)
Fig. 2. A part of lamprey ellipsoid, illustrating a mitochondrion with a fusion of internal
mitochondrial membranes (arrow) and with angulated cristae. Fixed in OsO4-Millonig's buffer,
stained with lead tartrate. (Original magnification x54,000.)
Fig. 3. Peculiar configuration of internal mitochondrial membranes cut nearly normal to the
plane of the membrane shown in higher magnification. Note the difference in thickness of intercristal (arrow J ) , intracristal (arrow 2), and intermitochondrial spaces (arrow 3). Fixed in
OsO4-Millonig's buffer, stained with lead tartrate. (Original magnification xll0,000.)
Fig. 4. Vertical section of the inner segment of a rod receptor cell of the giant salamander.
The ellipsoid consists of typical elongated mitochondria. However, in nearly all of these, the
lumen of the cristae are dilated in places and contain electron dense material (dc). OS, outer
segment; N, nucleus; G, Golgi complex. Fixed in glutaraldehyde-Millonig's buffer, postfixed in
OsO.i-Millonig's buffer, stained with lead citrate. (Original magnification xl8,000.)
Figs. 5 and 6. Ellipsoidal mitochondria of the giant salamander showing intracristal inclusions
which appear to be of very fine granules and helical filaments, respectively. Fixed in glutaraldehyde-Millonig's buffer, postfixed in Os04-Millonig's buffer, stained with lead citrate. (Original
magnification Fig. 5 x35,000, Fig. 6 x82,000.)
Fig. 7. Part of an ellipsoid of the toad rod receptor cell. Among the ordinary ellipsoidal mitochondria, large expanded mitochondria are filled with a mass of glycogen granules. A single or
small cluster of these can also be seen in the lumen of a crista (arrow). Specimen was fixed
in glutaraldehyde-OsO4-s-collidine buffer, stained with lead tartrate. (Original magnification
x26,000.)
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Atypical mitochondria in ellipsoid 305
\
Figs. 1-3. For legend see opposite page.
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\
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Investigative Ophthalmology
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306 Ishikawa and Yamacla
OS
N
Fig. 4. For legend see p. J04.
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Atypical mitochondria in ellipsoid 307
Figs. 5-7. For legend see p. 304.
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308 Ishikawa and Yamada
packed closely and in a fairly orderly
manner, that is, small typical ellipsoidal
mitochondria about 0.3 /A in diameter at
the periphery, and the larger unusual ones
more centrally. The mitochondria sometimes contain small osmiophilic granules.
These granules increase in number and size
(up to 0.2 ix in diameter) in the mitochondria located more centrally, and are arranged regularly along the mitochondrial
membranes or cristae (Fig. 10). Therefore,
one can discern more easily the irregular
outlines of mitochondria by tracing the
granules which are closely arranged in a
row.
Investigative Ophthalmology
June 1969
Depending on fixation or treatment with
saliva and RNAse, the electron density or
shape of these intramitochondrial granules
changed very slightly, nor was their size,
number, or pattern of distribution influenced. The snake ellipsoids, with such unusual mitochondria, stained intensely with
toluidine blue and showed a positive reaction for Sudan black B staining in histological preparations.
Another type of unusual ellipsoid was
found in one of the paired receptor cells
in the gecko retina and in cone cells of the
carp retina.
Although further histological study is
Text continued on p. 313.
Fig, 8. A nearly vertical section of a snake pure cone retina. Single cone (SE) and the principal
member of double cone (PE) have a large, barrel-shaped ellipsoid with a dense, granulated
core. On the other hand, the ellipsoid of an accessory cone (AE) consists of ordinary mitochondria, pe, Pigment epithelium; EM, external limiting membrane; OS, outer segment. Fixed
in OsOrMillonig's buffer, stained with lead tartrate. (Original magnification x4,000.)
Fig. 9. Cross-sectioned ellipsoid of a snake single cone. Typical ellipsoidal mitochondria are
located at the periphery of the ellipsoid. The more central mitochondria are larger and contain
small, osmiophilic granules. These granules are larger and more numerous in the mitochondria
toward the center of the ellipsoid. Fixed in OsOi-Millonig's buffer, stained with lead tartrate.
(Original magnification xl3,000.)
Fig. 10. Part of a modified mitochondrion of the snake ellipsoid at higher magnification. The
matrix of the extra large mitochondria is occupied by dense granules which are arranged in
rows along the mitochondrial membranes, mm, Outer and inner mitochondrial membranes;
cm, cristal membranes. Fixed in OsO-i-Millonig's buffer, stained with lead tartrate. (Original
magnification x64,000.)
Fig. 11. Modified mitochondria seen in cone ellipsoids of the carp retina. Large, irregularshaped mitochondria are almost completely converted to dense solid structures which are surrounded by mitchondrial double membranes (mm). In such mitochondria, only rudimentary or
small numbers of cristae (cm) can be seen along the mitochondrial membranes. Fixed in glutaraldehyde-OsO4-Millonig's buffer, stained with lead tartrate. (Original magnification x37,000.)
Fig. 12. "The Class B double" type photoreceptor cells of the gecko cut transversely through
a differentiated ellipsoid. Comparing an ordinary ellipsoidal mitochondrion with that of an
accessory member (AE). The ellipsoid of the principal member of the double cone contains a
large, lipidlike structure in the center region. Fixed in OsOi-s-collidine buffer, treated with
uranyl acetate in toto before dehydration, and stained with lead tartrate. (Original magnification x6,000.)
Fig. 13. Part of a differentiated ellipsoid of the gecko illustrating gradual alteration from the
typical mitochondrion to the lipidlike structure. This electron micrograph shows that the lipidlike structure at the center of ellipsoid is an extremely modified mitochondrion. Fixed in OsO^s-collidine buffer, treated with uranyl acetate in toto before dehydration, and stained with
lead tartrate. (Original magnification x25,000.)
Fig. 14. Low power electron micrograph of a turtle retina. In glutaraldehyde-fixed material,
oil droplets (OL) appear to be round or oval with very smooth outlines, pe, Pigment epithelium;
OS, outer segment; E, ellipsoid; P, paraboloid. Fixed in glutaraldehyde-OsO^-Millonig's buffer,
stained with lead citrate. (Original magnification x5,000.)
Fig. 15. Material from the same retina, as shown in Fig. 14, but fixed in osmium tetroxide. In
sharp contrast to Fig. 14, the oil droplet has a very irregular contour. Its surface is applied
closely to the surrounding mitochondria which have densely packed cristae. Fixed in OsO4Millonig's buffer, stained with lead citrate. (Original magnification xl9,000.)
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Atypical mitochondria in ellipsoid 309
Figs. 8 and 9. For legend see opposite page.
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310
Investigative Ophthalmology
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Ishikawa and Yamada
mm
-cm
Figs. 10 and 11. For legend see p. 308.
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Atypical mitochondria in ellipsoid 311
Figs. 12 and 13. For legend see p. 308.
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312
Ishikaioa and Yamada
Figs. 14 and 15. For legend see p. 308.
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needed, the photoreceptor cells of Gekko
•japonicus can be divided approximately
into two types. One appears as a twin or
triplet in which all members are equal and
ordinarily have a typical cone ellipsoid.
Another type is a pair of unequal cells with
exactly the same structure as ordinary
double cones except for the size and shape
of the outer segment. According to Underwood,7 these 2 types of visual cells may
correspond to the Class C double and the
Class B double cones, respectively. A specifically differentiated ellipsoid dealt with
in this paper was found in one of the
Class B double types.
Fig. 12 is a cross section of gecko retina
at the level of the differentiated ellipsoid
of the double receptor. Similar to the ellipsoidal pattern of the snake mentioned, the
structural feature of these ellipsoids differs
between the central and peripheral zones.
The first is occupied by large homogeneous
bodies with considerable election density.
They are more similar to a lipid droplet. In
both vertical and transverse sections, they
appear roughly spherical and extend from
the central to the distal region of the ellipsoid. However, closer examination reveals
that such spherical bodies are surrounded
by double membranes with rudimental cristae. In addition, transitional or intermediate forms are observed between typical
mitochondria at the vitreal end and spherical bodies at the scleral side (Fig. 13). In
other words, with the gradual loss of the
cristae, the density of the mitochondrial
matrix increases, suggesting the accumulation of some unusual material. These facts
indicate that the dense spherical bodies are
an extremely modified form of ellipsoidal
mitochondrion in which the majority of
the original mitochondrial components have
been replaced by a special substance. Exactly similar structures were found in the
cone receptor ellipsoids of the carp, Cyprinus carpio (Fig. 11).
Finally, observations on the photoreceptor cells with oil droplets will be described
briefly. Several variations of oil droplets,
colored or colorless, are located at the
Atypical mitochondria in ellipsoid 313
scleral end of the cone inner segment of a
great variety of vertebrates.2
Figs. 14, 15, and 16 are electron micrographs of receptor cells with oil droplets
in turtle and pigeon retinas. One can easily
distinguish these droplets by their various
densities. Some are quite dense while
others are less so, which probably represents differences in their composition that
are responsible for their color which is
recognizable in the fresh material.
The most interesting feature of the oil
droplets is their shape. In osmium-fixed
material, the oil droplets have a rather
irregular contour, whereas those prefixed
with glutaraldehyde are round or oval
with a very smooth outline. Such sharp
contrast in shape was well demonstrated in
the oil droplets of the turtle, Clemmys
japonica, shown in Figs. 14 and 15.
Regardless of the manner of preparation,
the ellipsoid substance is in intimate contact with an oil droplet, mainly on its
vitreal surface. As seen in Fig. 15, the mitochondria sometimes appear to adhere closely to oil droplets so that the outer mitochondrial membrane in the region of contact seems to have disappeared.
Ellipsoidal mitochondria accompanied by
oil droplets were typical in all cases. They
had densely packed cristae and no structural modification or other observable differentiation.
Discussion
The mitochondria in retinal ellipsoids,
for example, those in human photoreceptor
cells,3 are typically long and slender and
are arranged in rows parallel to the axis
of the inner segment. However, there are
several variations in vertebrate retinas. In
some cases, the variation appears in one
individual mitochondrion in an ellipsoid,
and in others, the ellipsoid as a whole is
differentiated into regions characterized by
special mitochondria. The ellipsoidal mitochondria in the lamprey, giant salamander,
and toad belong in the former category,
while the gecko, carp, and snake ellipsoids
belong in the second.
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tstigative Ophthalmology
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314 Ishikawa and Yamada
Fusion occurring between membranes of
the cristae themselves and the inner mitochondrial membrane in the lamprey ellipsoid resembles somewhat the fine structure
of grana in the chloroplast of plant cells.s
Similar structures have not been reported
so far in any mitochondria. They are found
in nearly all receptor cells in each lamprey
retina so far examined, regardless of the
methods of fixation employed. Therefore,
this structure may hardly be regarded as
an artifact.
As is shown in Fig. 3, the fusion occurred always between the outer surface of
adjacent cristae, or between the mitochondrial inner membrane and the outer sur-
face of cristae; therefore, the intercristal
spaces disappeared in these places. No
membrane fusions were recognized involving the outer mitochondrial membranes.
These findings may indicate an asymmetrical structure of the outer and inner mitochondrial membranes. The question is
raised whether there is any change in the
macromolecular composition of such fused
regions. Are there any elementary particles
in the region of such fused membranes?
These are unsolved problems.
Whereas the granulated inclusion bodies
in the intracristal lumen of ellipsoidal mitochondria of certain photoreceptor cells
were identified as glycogen, the chemical
16
Fig. 16. Vertical section of inner segments or pigeon photoreceptors. The dillerence in electron
density of an oil droplet can be observed. Small, dense granules (sg) are only found in the
receptor cells which possess large oil droplets with hollow cores. Fixed in OsCX-s-collidine
buffer, treated by uranyl acetate as a block before dehydration, stained with lead tartrate.
(Original magnification xl3,000.)
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nature of the intracristal amorphous substance and filaments with helical substructure seen in giant salamander ellipsoids is
unknown. The intramitochondrial glycogen
granules, as well as intramitochondrial inclusions in various forms, filamentous or
crystalline, have been reported in a number
of different cell types and organisms.0"11
The presence of DNA fibrils12 or insoluble
inorganic salts13 has been well established
recently. Thus, accumulation of special substances in mitochondria would not be specific features for ellipsoidal mitochondria,
but rather common phenomena for mitochondria in general. However, the functional significance of the intracristal material in the ellipsoidal mitochondria is still
unknown.
In contrast, the characteristic ellipsoids
of receptor cells in the gecko, carp, and
snake can be assumed to be a specifically
differentiated form with relation to visual
perception. The fine structures of the retinal
oil droplets, reported by several authors,
can be classified into two types. In Type I,
the oil droplet is more like the lipid droplets in other cell types; it shows a homogeneous internal structure with various densities, such as those in the frog,14 diurnal
gecko,15 and pigeon.10 Type II is one which
was reported by Berger17 in the guppy
double cone inner segment. It is bounded
by a double membrane, and is vesicular or
granular in internal structure. In his paper
Berger concluded that mitochondria at the
scleral end of ellipsoids differentiate into
oil droplets. However, the observation on
the developing chick retina which contains
Type I oil droplets in mature form reveals:
(1) that oil droplets are already found as
small droplets at early developmental stages
when the apical region of visual cells has
started to differentiate into inner segments,
and (2) that direct transformation from
mitochondria to oil droplets, as described
in the case of the guppy, is not apparent
throughout the developmental stages of
photoreceptor cells in the chick, despite
the close topographical relationship between them (unpublished observation).
Atypical mitochondria in ellipsoid 315
Thus, oil droplets of Type I and Type II
are entirely different entities in their structure, as well as in their morphogenesis.
The structural features of the modified
mitochondria in the specially differentiated
ellipsoids of the gecko, carp, and snake are
similar to those associated with the Type II
oil droplet described by Berger. Since such
modified mitochondria are still bounded by
a double membrane, possess rudimental
cristae, and are intermediate between the
typical mitochondria and the modified ones,
whether it is reasonable to designate them
as "oil droplets," as was done in Berger's
paper, is still questionable. However, numerous intramitochondrial granules in the
snake photoreceptor ellipsoid contain a
Sudan black B positive substance, and the
modified mitochondria in the gecko and
carp have structural similarity to lipid droplets in many cell types. In addition, no
ordinary oil droplets exist within such a
differentiated ellipsoid. These findings lead
us to speculate that such ellipsoids as a
whole may function as oil droplets, since
each modified mitochondrion maintains its
individuality in the ellipsoid. More specifically, the ellipsoid of certain animal visual
cells may be assumed to have a dual functional significance, namely, as a source of
energy for the photoreceptor cell, and to
function as an oil droplet.
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