Pineal organs of deep-sea fish: photopigments and structure
1 Division of Visual Science, Institute of Ophthalmology, University College
London, London EC1V 9EL, UK
2 Graduate School of Neural and Behavioural Sciences, Max Planck Research
School, Anatomisches Institut, Universität Tübingen, D-72074
Tübingen, Germany
* Author for correspondence (e-mail: j.bowmaker{at}ucl.ac.uk)
Accepted 19 April 2004
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Summary |
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Key words: photopigment, pineal organ, pinealocyte, pineal pigment, morphology, fish
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Introduction |
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Pineal photoreceptors function primarily as luminance detectors, since the
lack of any focussing mechanism and the irregular organisation and
convolutions of the pineal epithelium mean that only diffuse light reaches the
pineal. In addition, the high convergence of photoreceptors to neurons and the
slow time course of pineal photoreceptor responses
(Marchiafava and Kusmic, 1993;
Meissl and Ekström, 1988
)
imply that the pineal cannot distinguish discrete, rapidly changing light
stimuli. The pineal is thus designed to detect slowly changing ambient light
levels, ideal for the photic control of circadian and seasonal behaviour
(Ekström and Meissl,
1997
).
There is limited information as to the photosensitive pigments of pineal
organs and, in teleosts, this is restricted to a small number of species
representing only a few of the major teleost families. In salmonids,
electrophysiological data from various species of trout and salmon have
identified at least two `pigments' with max close to 530
and 500 nm (Marchiafava and Kusmic,
1993
; Meissl and Ekström,
1988
), but microspectrophotometric measurements have identified
pigments with
max at about 460 and 560 nm
(Kusmic et al., 1993
).
Similarly, in the pike (Esox lucius; Esocidae), there are potentially
three pigments with
max at
380, 530 and 620 nm
(Falcón and Meissl,
1981
). In these species, there is evidence for a chromatic output
from the pineal. By contrast, data from the cyprinids suggest that only a
single photopigment with
max close to 530 nm is present
(Meissl et al., 1986
;
Nakamura et al., 1986
).
Because of the indirect methods employed, the assumption has been that even
though the
max of these pigments were somewhat different
from those of the visual pigments, the pineal was expressing either rod or
cone pigments or both. These data are supported by studies using
immunocytochemical labelling of pineal photoreceptors, employing a range of
antibodies (e.g. COS and OS) raised against retinal opsins
(Forsell et al., 2001
;
Garcia-Fernandez et al., 1997
;
Tamotsu et al., 1994
;
Vigh-Teichmann et al., 1990
,
1992
), which again indicate
that both rod-like and cone-like opsins may be present.
Recently, a number of additional opsins have been identified in vertebrates
that are not expressed in either retinal rods or cones and that belong to
opsin families distinct from the rod and four classes of cone opsin. At least
two of these, VA opsin (Foster and
Hankins, 2002; Kojima et al.,
2000
; Moutsaki et al.,
2000
; Soni and Foster,
1997
) and parapinopsin
(Blackshaw and Snyder, 1997
),
have been located in areas associated with the teleost pineal. However, a more
specific teleost pineal opsin, `exo-rhodopsin', has been identified in
zebrafish, Danio rerio (Mano et
al., 1999
), or `extra-retinal rod-like opsin' (ERrod-like opsin)
in Atlantic salmon (Salmo salar) and puffer-fish, Fugu
rubripes (Takifugu rubripes)
(Philp et al., 2000
). This
opsin, assumed to be ubiquitous in teleosts, clearly belongs to the rod opsin
family but is not expressed in the retina
(Bellingham et al., 2003
). The
term `ERrod-like opsin', though cumbersome, is preferable, since it avoids the
confusion that `exo-rhodopsin' can introduce, given that pineal pigments may
be either rhodopsins or porphyropsins, i.e. based on vitamin A1 or
vitamin A2.
Photopigments, presumed to be ERrod-like opsins, have been measured by
microspectrophotometry in a cyprinid, the goldfish (Carassius
auratus; Peirson and Bowmaker,
1999), and a characid, the cavefish (Astyanax fasciatus;
Parry et al., 2003
). In the
goldfish, where the retinal pigments are all porphyropsins, the rods have
max at 522 nm, whereas the pinealocytes appear to have a
mixed pigment pair based on retinal and 3-dehydroretinal with a
max close to 512 nm
(Peirson and Bowmaker, 1999
).
Astyanax, which also has retinal pigments that are
A1/A2 mixtures, similarly has pinealocytes with
max at shorter wavelengths than the rods
(Parry et al., 2003
). In both
species, no additional photopigments were identified in the pineal organ.
In mesopelagic fish from depths just within the reach of sunlight, the
pineal organ is ideally situated to monitor the intensity of the down-welling
daylight. Typically, the pineal end-vesicle is located underneath a
conspicuous `window' in the skull where the skin lacks melanophores and the
skull shows a distinct thinning (McNulty,
1976; McNulty and Nafpaktitis,
1977
). This is accompanied by an increase in size of the
photoreceptor outer segments, including the number of discs, presumably to
increase sensitivity to the very dim light at depth.
We have examined the photopigments and morphology of the pineal organs from
a number of mesopelagic fish including representatives of the hatchet fish
(Sternoptychidae), scaly dragon-fish (Chauliodontidae) and bristlemouths
(Gonostomidae). We also investigated the pineal of the deep demersal eel,
Synaphobranchus kaupi (Wagner and
Mattheus, 2002). In all cases, a pineal photopigment was detected
that was spectrally distinct from the retinal rod pigment and has a
max displaced to longer wavelengths. In one species of
hatchet fish, Argyropelecus affinis, two spectral classes of
pinealocyte were identified, both spectrally distinct from the retinal rod
photopigment.
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Materials and methods |
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Histology
Pineal glands were isolated, preferably with parts of the cranium attached,
and fixed in a mixture of 4% paraformaldehyde, 2% glutaraldehyde in 0.1 mol
l-1 cacodylate buffer
(Karnovsky, 1965). All samples
were stored at 4°C until further processing back on land. After thorough
washing in buffer, the pineals were postfixed in 1% osmium tetroxide (2 h),
blockstained with 1% uranyl acetate and embedded in Epon. Short series of 1
µm sections were cut alternating with ultrathin (80 nm) sections. Digital
micrographs were obtained with a Zeiss Axioskop and a LEO EM912.
Microspectrophotometry
All procedures were carried out under dim red light. Pineal organs were
recovered by removal of the dorsal surface of the cranium and, in most cases,
the whole piece of cranium including the pineal organ was stored. Tissue was
lightly fixed in a 2% glutaraldehyde solution for 1530 s, washed
in saline and then stored at 4°C in saline containing antibiotic and
antimycotic agents (streptomycin and amphotericin; Sigma Chemical Co.). In
London, the lightly fixed pineal organs were removed from the skull and teased
apart on a coverslip with fine needles. The dispersed tissue was mounted in
marine saline containing 5% or 10% dextran and squashed with a second
coverslip, which was sealed with wax.
Microspectrophotometric recordings were made in the conventional manner
using a Liebman dual-beam microspectrophotometer
(Bowmaker et al., 1991;
Liebman and Entine, 1964
;
Mollon et al., 1984
). Spectra
were recorded at 2-nm intervals from 750 to 350 nm and from 351 to 749 nm on
the return scan. The outward and return scans were averaged. A baseline
spectrum was measured for each cell, with both beams in an unoccupied area
close to the cell, and this was subtracted from the intracellular scan to
derive the final spectrum. Two baseline scans were recorded for each cell and
averaged. All cells were bleached with white light for 2 min, and post-bleach
spectra were recorded. The
max of both the absorbance
spectra and difference spectra were determined by a standard computer
programme that best fits a visual pigment template to the right-hand limb of
the spectra (Bowmaker et al.,
1991
; Mollon et al.,
1984
). Selection criteria were used to discard records either with
low absorbance or in which the difference spectrum was clearly distorted.
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Results |
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The low-power micrograph of the pineal of another hatchet fish,
Argyropelecus affinis, shows the flattened vesicle in close
apposition to the cartilaginous skull (Fig.
1d). The vesicle wall is formed by a folded epithelium of
irregular width. The basal lamina shows a number of infoldings, and the spaces
thus created are occupied by numerous blood vessels
(Fig. 1e). On the apical
(luminal) side, numerous elongated profiles protrude into the vesicle lumen;
sometimes they show an hourglass-like constriction in the middle, separating
the inner and outer segments of the photoreceptors. Apart from photoreceptors
that border the lumen and have mostly spherical and lighter nuclei, at least
one additional cell type is present in this epithelium, which is characterised
by a darker-staining cytoplasm and nucleus. The outer segments contain a stack
of 30 discs that overall form a conical structure with an extension of
the inner segment in the centre (tangential section:
Fig. 1f). On the external
(basal) surface of the pineal vesicle, cells with a more electron-dense
cytoplasm are found, containing bundles of neurofilaments and lobulated nuclei
with conspicuous clumps of heterochromatin.
In contrast to the two previous species, in the bristlemouth Gonostoma elongatum, the pineal epithelium is composed of a continuous sheath of tall columnar cells (Fig. 1g). The photoreceptor outer segments resemble those in the other mesopelagic fish. Blood vessels are located outside the smooth basal surface. In the vicinity of the capillaries, the surface of the basal plasma membrane of the external cells is greatly enlarged by numerous infoldings. In the dragon-fish Chauliodus sloani, the thin wall of the pineal vesicle appears to be perforated by numerous dilated capillaries, around which the sensory epithelium is wrapped (Fig. 1h). The concentric whorls of outer segment discs contain about 20 lamellae. Basal cells are more electron dense and contain lobulated nuclei with numerous clumps of heterochromatin. Their basolateral aspect is smooth and shows little infolding.
Microspectrophotometry
Measurements began a few weeks after collection and, in this `early'
tissue, high densities of pigments were measured in the pinealocytes, but with
rising absorbance at short wavelengths
(Fig. 2A). The data were all
best fitted to a vitamin A1 (rhodopsin) template. Estimates of
max from both the absorbance spectra and the difference
spectra were similar, within about 3 nm of each other. With increasing storage
times, the density of pigment decreased with a significant rise in shortwave
absorbance (Fig. 2B), making
use of the absorbance spectra for estimates of
max somewhat
unreliable. However, even after 12 months of storage, clear difference spectra
could still be obtained after bleaching and no `empty' pinealocytes were
identified. The absorbance at short wavelengths had triple peaks
characteristic of carotenoids and it is assumed that the yellow pigmentation
in the antimycotic/antibiotic storage medium had become bound to the pineal
tissue. Because of the need to use difference spectra to obtain reliable
max from the older tissue, data from all the species have
been tabulated in this form to aid comparisons.
|
Photosensitive pigments were measured from the pinealocytes from all eight
species. Full details of the number of fish and the max of
the pigments are listed in Table
1, along with previously published data for the rod visual
pigments (with reference sources). Histograms of the distribution of the
max of individual cells are presented in
Fig. 3. In every case, the
pineal pigments had
max at longer wavelengths than the
published data for retinal rod visual pigments. In seven of the species, only
a single pineal pigment was detected. However, in one species,
Argyropelecus affinis, the distribution of the
max
of the individual cells (Fig.
3) indicated a bimodal population with spectrally distinct
pigments recorded from separate populations of pinealocytes, although no
morphological differences could be identified. This division was apparent in
four of the five individuals studied. The distribution of
max has been arbitrarily divided at 490 nm (the minimum
point in the histogram and the region of greatest spectral separation),
yielding two pigments with
max at
486 and 498 nm
(Fig. 4). Both pigments have
max at longer wavelengths than the retinal rod visual
pigment (Table 1).
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Within the hatchet fish, the genera Sternoptyx and
Argyropelecus have retinal rod pigments with max
at
478 nm, whereas the
max of the pinealocytes are
close to 486 nm and 497 nm. A further species, Polyipnus polli, has a
rod pigment with
max at 483 nm and a 500-nm pinealocyte
pigment. The bristlemouth Gonostoma elongatum has pigments very
similar to those of P. polli, as does the scaly dragon-fish,
Chauliodus sloani, with the rod and pineal pigments at 485 and 503
nm, respectively (Table 1).
In marked contrast, the deep-sea demersal eel, Synaphobranchus
kaupi, although having a typical deep-sea rod pigment with
max at
478 nm, possesses a pineal pigment displaced
some 37 nm to longer wavelengths, close to 515 nm.
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Discussion |
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The most striking feature of the photosensitive pigments of the pineal organs of these deep-sea fish is that the pigments are clearly spectrally distinct from the retinal rod pigments, the only visual pigment present in the pure rod retinae of these species. In all cases, the pineal pigment absorbs at longer wavelengths.
The pineal organs of these deep-sea fish do not appear to express the
retinal rod opsin gene but presumably express the closely related ERrod-like
opsin gene, which is expressed uniquely in the pineal
(Bellingham et al., 2003;
Mano et al., 1999
;
Philp et al., 2000
). An
ERrod-like opsin has not been experimentally expressed and reconstituted
in vitro for any teleost species, so that any relationship between
the
max of the rod pigment and the ERrod-like opsin has not
been established. However, presumed ERrod-like opsins have been measured by
microspectrophotometry in shallow-living freshwater cyprinids such as goldfish
(Peirson and Bowmaker, 1999
),
orfe (Leuciscus idus; S. N. Peirson and J. K. Bowmaker, unpublished
observations) and a characid, the cavefish (Astyanax fasciatus;
Parry et al., 2003
). In the
goldfish, where the retinal pigments are all porphyropsins, the rods have
max at 522 nm whereas the pinealocytes appear to have a
mixture of pigments based on retinal and 3-dehydroretinal with a
max close to 512 nm. By contrast, in the orfe, the
pinealocytes have
max that are 1520 nm longer
(
max
534 nm) than the rods (
max=517
nm). Astyanax is more similar to goldfish, with pinealocytes having
max at shorter wavelengths, although the
max varies between individual fish because of variation in
the ratio of A1:A2 chromophores. The rod and pineal
pigments have
max at 511535 nm and 503518 nm,
respectively (Parry et al.,
2003
). In all three species, no additional photopigments were
identified in the pineal organ.
There is a superficial correlation between the max of
the rods and pineal pigments in the deep-sea pelagic species: as the
max of the rods shifts to shorter wavelengths, so do those
of the pinealocytes. However, this trend is not maintained in the demersal
Synaphobranchus, where the pineal pigment is some 37 nm longer than
the P478 of the retina. It is somewhat paradoxical that the pineal pigment
should be so long-wave shifted in such a deep-water species.
The max of rod visual pigments of deep-sea fish tend to
cluster at specific spectral locations
(Dartnall and Lythgoe, 1965
;
Partridge et al., 1989
) and
the basis for this lies in specific amino acid substitutions within the opsins
of the pigments that cause clearly defined spectral displacements
(Hunt et al., 2001
). Although
the amino acid sequences of the pineal pigments reported here have not been
determined, their spectral locations, close to cluster points of the deep-sea
rod pigments, strongly suggest that they too will show similar mechanisms of
spectral tuning.
It is not apparent why the pineal and rod photopigments in deep-sea fish
should be spectrally distinct. It has long been argued that the rod pigments
of deep-sea fish are spectrally tuned to match the maximum irradiance of the
down-welling daylight and/or the maximum emission of the majority of
bioluminescence (for recent reviews, see
Douglas et al., 1998;
Partridge and Cummings, 1999
).
However, it could also be argued that the pineal organs should similarly be
spectrally tuned to be maximally sensitive to the down-welling light, but
clearly both photopigments cannot be tuned to the same stimulus. Although we
have no data on the transparency of the pineal `window' in these deep-sea
fish, it is unlikely that prereceptoral filtering would change the spectral
sensitivity greatly, since the `window' is composed of a thin layer of bone
and skin pigmentation, which will be spectrally relatively neutral, causing
scattered and diffuse light to reach the pinealocytes.
There is sufficient daylight in the open ocean to support scotopic vision
in deep-sea fish to depths perhaps as great as 1000 m
(Clarke and Denton, 1962),
where the intensity of sunlight is reduced by
10-12 from that
at the surface. However, scotopic vision, whether the ability to detect a
moving object silhouetted against the down-welling background space light or
to detect bioluminescence, is concerned with transient moving stimuli. The rod
neural pathway has a relatively short integration time in the millisecond to
second range, along with the ability to adapt to changes in the background
illumination (e.g. Arshavsky et al.,
2002
; Lamb and Pugh,
1990
). This appears not to be the case with the pineal. Pineal
photoreceptors respond to relatively long-duration flashes in a similar manner
to rods, with an amplitude-coded hyperpolarization, although the response has
a much slower time course, with increased latency, time to peak and recovery.
However, they behave differently to prolonged illumination (50 s), with the
photoresponse maintained at the same amplitude for the whole duration of the
illumination (Kusmic et al.,
1992
). The system thus appears to be designed to integrate over a
considerable time scale with a sustained signal output and without adaptation.
Because of this, it would seem likely that the pineal organs of deep-sea fish
may well be able to function at light levels similar to or even lower than the
levels required for scotopic vision. Short transient bursts of bioluminescence
will go undetected, but small diurnal changes in the intensity of the space
light may be detected at depths equal to or greater than the limits of
scotopic vision.
While it is conceivable that the pineal organs of mesopelagic fish are
capable of capturing photons of solar origin, this is less likely for the
bottom-living eel, which not only lives outside the reach of sunlight but also
has no epidermal or cranial window. It is therefore highly unlikely that the
well-developed pineal photoreceptors are exposed to any kind of light. Yet one
of the main functions of the pineal organ, namely the secretion of melatonin,
has been demonstrated in culture experiments in S. kaupi and some
mesopelagic species (H. J. Wagner, K. Kemp, U. Mattheus and I. G. Priede,
manuscript in preparation). One may therefore wonder why pineal organs with a
`complete' set of morphological features and functional visual pigments are
found in these eel specimens and, perhaps, also in the other deep-sea fish. A
possible reason for this paradox may lie in the ontogeny of these fish. As a
general rule, deep-sea fish spend their early lives in the upper mesopelagic
or even epipelagic zone. Typically, their larvae (leptocephali) are
transparent, a camouflage strategy that only makes sense in a `visual
environment'. This is also true for the eel S. kaupi, the eggs of
which develop off the southern east coast of North America, and the larvae of
which drift at depths between 100 and 270 m over a period of up to two years
towards the Eastern North Atlantic
(Marshall, 1954). Since pineal
photoreceptors in fish start to differentiate even prior to retinal ones
(Ekström and Meissl, 1997
;
Negishi and Wagner, 1995
), it
is feasible to assume that pineal organs in the eel, but probably in deep-sea
fish in general, develop in a photic environment and differentiate to assume a
photosensory function in their early life history, similar to surface-dwelling
fish. When they start their migration towards their non-photic adult habitats,
the structural and functional features are retained and are not abandoned
during metamorphosis. Although they are deprived of photic stimulation, their
main role of melatonin synthesis is active, thereby synchronising the
biological rhythms of various organ systems. Since solar light can no longer
act as a zeitgeber, alternative temporal cues such as changing water current
direction, not transduced by the pineal, may become effective.
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Acknowledgments |
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