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First published online August 31, 2007
Journal of Experimental Biology 210, 3179-3187 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002394
Serotonin and nitric oxide interaction in the control of bioluminescence in northern krill, Meganyctiphanes norvegica (M. Sars)
1 Department of Zoophysiology, Göteborg University, Box 463, SE 405 30
Göteborg, Sweden
2 Kristineberg Marine Research Station, SE 450 34 Fiskebäckskil,
Sweden
3 Lab Marine Biology, Catholic University of Louvain, B-1348
Louvain-la-Neuve, Belgium
* Author for correspondence (e-mail: jenny.kronstrom{at}zool.gu.se)
Accepted 28 June 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: bioluminescence, 5-HT, Meganyctiphanes norvegica, nitric oxide, nitric oxide synthase, krill
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Herring and Locket,
1978). Various adaptive benefits have been suggested for this
phenomenon, including camouflage through counter shading and communication
between individuals. Experiments have shown that krill respond to different
types of light stimuli with light production of their own (light-induced light
reaction) (Mauchline, 1960;
Kay, 1965).
The northern krill (Meganyctiphanes norvegica) produces light from
10 separate light organs (photophores): one on each eyestalk, two pairs on the
ventral thorax and four separate organs under the abdomen
(Herring and Locket, 1978).
The control of light emission in these animals is not well studied, but
serotonin (5-hydroxytryptamine, 5-HT) is known to stimulate light production
or to increase the sensitivity to light gradients
(Kay, 1962;
Fregin and Wiese, 2002),
although the mechanism for this is unknown. The putative light-producing cells
(photocytes) are not innervated; instead, nerves follow capillaries inside the
photophore and innervate a sphincter-like structure at the base of a second
cell-type located close to the assumed photocytes in the light-producing
structure (lantern) (Fig. 1)
(Petersson, 1968;
Herring and Locket, 1978).
|
). Light
production in the firefly is initiated when specific cells closely associated
to the photocytes are stimulated by octopamine to produce nitric oxide (NO).
NO in turn stimulates flashing by inhibiting photocyte respiration, thereby
leaving oxygen free for the light reaction
(Trimmer et al., 2001). NO has
also been suggested to be involved in the control of light production in the
fish Argyropelecus hemigymnus, where it has a modulatory effect on
adrenaline-stimulated bioluminescence
(Krönström et al.,
2005).
The signalling molecule NO is involved in many different physiological
processes, including vasodilation, immune defence, neurotransmission and
neuromodulation, in vertebrates as well as invertebrates
(Bredt and Snyder, 1992;
Bredt and Snyder, 1994;
Colasanti and Venturini, 1998;
Torilles, 2001). It is a
molecule with a short half-life that can diffuse through cell membranes and
have different intracellular effects. In many systems, the physiological
effects of NO are mediated through the production of cyclic guanosine
monophosphate (cGMP), by stimulation of the enzyme guanylyl cyclase in the
target cell (Jacklet, 1997).
NO can also control physiological mechanisms in the target cell by inhibiting
mitochondrial respiration through a cGMP-independent pathway
(Brown, 1994). Evidence for the
presence of the enzyme nitric oxide synthase (NOS) in the nervous system of
different crustacean species has been presented by several authors using
antibodies against NOS and/or NADPH-diaphorase histochemistry
(Scholz et al., 2002;
Zou et al., 2002;
Christie et al., 2003).
Based on the morphological similarities of the krill and the firefly light organs as well as the properties of the NO molecule outlined above, we hypothesized that NO might be involved in the control of light production in krill. This possibility was investigated both by functional studies of light production in living animals and with immunohistochemistry using antibodies raised against NOS.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Immunohistochemistry
Method
Abdominal photophores from 21 krill were dissected out and fixed for
1–24 h in Zamboni's fixative (15% picric acid, 2% formaldehyde in
phosphate-buffered saline) (PBS, 0.9% NaCl, pH 7.2) or 1–4 h in
paraformaldehyde (PFA) [3.7% PFA in phosphate buffer (PB), pH 7.2].
Zamboni-fixed preparations were washed repeatedly in 80% ethanol, and the
tissue was dehydrated (95% and 99.5% ethanol, 30 min each), which allows
penetration of xylene. Treatment with xylene was made (30 min) to remove
tissue fats, and the preparations were then rehydrated (99.5%, 95%, 80% and
50% ethanol, PBS, 30 min each) for storage. Preparations fixed in PFA were
rinsed for 30 min in PBS. All preparations were stored overnight in PBS with
30% sucrose, before they were embedded in OCT (Sakura, Zoeterwude, The
Netherlands) or agarose (Sigma Chemical Company, St Louis, MO, USA) and quick
frozen in isopentane chilled with liquid nitrogen. Frozen samples that were
not cut immediately were stored at –40°C until use.
A cryostat microtome (Zeiss Microm International GmbH, Walldorf, Germany) was used to cut 10–20 µm sections, which were captured on chrome alum gelatine-coated slides and left overnight to dry. The slides were stored at –20°C until use.
Antibodies
Antibodies against all (mammalian) isoforms of NOS [neuronal, inducible and
endothelial NOS (nNOS, iNOS and eNOS);
Table 1] were used in
preliminary tests to detect NOS-immunoreactive material in sections of
abdominal photophores. Antibodies against nNOS and the universal NOS antibody
revealed NOS-like immunoreactivity (NOS-LI IR) in structures inside the
photophores in similar, but not identical, patterns of labelling. No staining
was detected with the antibodies against iNOS and eNOS.
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The antigen sequences against which the different primary antibodies are
raised were compared with the most related NOS sequence available, i.e. that
of a crustacean, Gecarcinus lateralis
(Kim et al., 2004), using the
program ClustalW to establish the theoretical fit to a possible krill NOS. The
antigen sequences for all the antibodies that showed staining in our
experiments show significant alignments with G. lateralis NOS. The
best agreement (100%) was obtained with the universal NOS (uNOS)-antibody
(PA1-039), which is also most commonly used in studies of invertebrates
(Scholz et al., 2002;
Christie et al., 2003). The
uNOS antibody was therefore judged to be the most likely to show genuine NOS
IR, and results from further tests are reported from this antibody only.
An antibody against 5-HT was used to establish the presence of structures containing 5-HT in the photophores (Table 1).
To reduce non-specific staining, sections were preincubated with normal
donkey serum (10% in PB with 2% NaCl, 0.1% bovine serum albumin, 0.2%
NaN3 and 0.2% Triton X-100) for 30–60 min. Primary antibodies
(Table 1) were applied and the
sections incubated for 24 h. The sections were rinsed (3x5 min in PB
with 2% NaCl) and incubated for 60 min with the secondary antibody conjugated
either to a fluorophore or to biotin (Table
1). All incubations were made in a humid chamber at room
temperature (
20°C).
The preparations with fluorophore-conjugated secondary antibodies were rinsed again as described above and mounted in Vectashield mounting medium (Vector Laboratories, Burlingame, CA, USA), then examined using a Nikon Eclipse E1000 microscope (Nikon, Tokyo, Japan) equipped with a Nikon DMX1200 digital camera. Captured images were processed with Adobe Photoshop.
Sections treated with biotinylated secondary antibodies were incubated with avidin-biotinylated peroxidase complex (ABC Elite PK 6100 standard; Vector Laboratories) for 30 min and either subsequently developed in Vector Nova red substrate kit (SK 4800; Vector Laboratories) for 3 min or incubated with fluorophore-conjugated streptavidine (SA-488, working dilution 1:2000; Molecular Probes, Eugene, OR, USA) for 1 h. The sections were mounted in 50% glycerol and 50% carbonate buffer (pH 8.5) or Vectashield mounting medium and examined as described above.
Controls performed to confirm the specificity of the secondary antibodies, by omission of the primary antibody, did not reveal non-specific staining with any of the secondary antibodies in the test.
Pharmacology
Chemicals
Stock solutions of 8-Bromoguanosine 3',5'-cyclic monophosphate
sodium salt monohydrate (8BrcGMP), 5-hydroxytryptamine hydrochloride (5-HT),
NG-nitro-L-arginine methyl ester (L-NAME) and
sodium nitroprusside (SNP) (all purchased from Sigma Chemical Company) were
prepared in crustacean saline (Holmes et
al., 1999) containing (in mM l–1): 478.0 NaCl;
12.74 KCl; 13.69 CaCl2 2H2O; 20.47 MgSO4
6H2O and 3.9 Na2SO4 (all purchased from Merck
KGaA, Darmstadt, Germany), and 5.0 HEPES (Sigma); pH was adjusted to 7.45.
S-nitroso-N-acetylpenicillamine (SNAP; Sigma) was prepared in distilled water
and (1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one) (ODQ; Sigma) in dimethyl
sulfoxide (DMSO).
Method
Live krill were used in the pharmacological experiments. Individual
specimens were placed in plastic vials containing 10 ml of deep-sea seawater
and exposed to light (12 µmol photons m–2
s–1, LI 1000 Datalogger; LI-COR, Lincoln, NE, USA) for 1 h.
This was done to standardize the light exposure of each specimen prior to the
experiments. Earlier studies have shown that M. norvegica is
stimulated to produce light both by short light flashes and more prolonged
exposure to light (Mauchline,
1960; Kay,
1965).
After light pretreatment, the vial containing the krill was placed in a
luminometer [Berthold FB12 (Pforzheim, Germany) calibrated with a standard
light source, 470 nm (Betalight, SRB Technologies, Winston-Salem, NC, USA)]
and the light-stimulated light response was recorded. When the response had
subsided the animal was injected in the pleon (the tail musculature) as
described by Fregin and Wiese (Fregin and
Wiese, 2002) with test substance (5 µl) using a Hamilton
syringe and the subsequent response measured. All test substances were
injected except ODQ, which was dissolved in DMSO (Merck, Germany) and applied,
giving a final concentration of 0.1% DMSO in the vial containing the
krill.
Temperature during the measurements was kept low either by performing the experiments in a temperature-controlled room (at 6°C) or by changing the water in the vial before injecting the test substance. Responses to 5-HT (Ltot, see below for definition), which were used as control, did not differ significantly between the methods.
Calculations and statistics
Each light response after injecting either 5-HT or 5-HT in combination with
an NO donor or a NOS inhibitor was characterized by three parameters
calculated as constants of a Gompertz equation of an asymmetrical growth curve
estimated by least-square method from the original data
(Fig. 2). The calculated
parameters were Ltot, the total amount of light in quanta
(q s–1); RLPmax, maximum rate of light
production (q s–2) (the maximum growth rate of the curve at
inflection point, ip); tip, time to the ip in seconds:
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0.03 mmol l–1) is in the lower range for
triggering light production. Earlier studies show that concentrations lower
than 0.01 mmol l–1 in the haemolymph induced a feeble or no
light response in M. norvegica
(Fregin and Wiese, 2002).
In treatments without 5-HT (saline control or nitrergic drugs) the integrated light production for 10 minutes at the peak of response was used for comparisons between treatments.
Each mean value is expressed with its standard error of the mean (mean
± s.e.m.); analysis of variance (ANOVA), t-test, Dunnet and
Bonferroni tests were used to determine significant differences between the
groups. All methods were designed under the assumption that the data are
normally distributed. Shapiro and Wilk statistics were used to check that the
data were a random sample from a normal distribution
(Shapiro and Wilk, 1965). When
data were not normally distributed or when unequal variances occurred, a log
transformation of data was performed as indicated by Sokal and Rohlf
(Sokal and Rohlf, 1995).
Analyses were performed using SAS/STAT® software's capabilities
(SAS Institute Inc., 1990) or
GraphPad Prism, version 4.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Herring and Locket, 1978).
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NOS
The universal NOS antibody revealed NOS-like IR of vessels or the area
around vessels, primarily at the border of the lantern where the vessels
connect to the C-cells before draining into the lantern
(Fig. 4A), but also in the
periphery of the light organ (Fig.
4B). Staining is most clear in cross-sections of the C-cells, as
described above. Moreover, staining is detected beside the lens, possibly at
the entry point for the photophore arteries
(Fig. 4C).
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Pharmacology
The effects of the NO donors SNP and SNAP, the NOS inhibitor
L-NAME, a membrane-permeable cGMP-analogue (8BrcGMP) and ODQ, an
inhibitor of guanylyl cyclase, on the light production from M.
norvegica photophores were investigated. 5-HT was used as a positive
control and to induce light production. Saline was used as a negative
control.
Controls: 5-HT and saline
Injections of 5-HT (resulting in 0.03 mmol l–1 in the
haemolymph) stimulated a light response, which typically lasted at least 15
min. The accumulated total amount of light emitted (Ltot)
in response to 5-HT seems to vary over the year. In April and June the average
Ltot appeared to be higher than in the autumn and winter
months because of a few specimens with a very high response
(Fig. 5). Below, the results
from treatments with NO donors and NOS inhibitors are compared with 5-HT
controls performed at the same time of year. Injections of saline only
occasionally evoked a minor light response
(Table 2).
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NO donors and NOS inhibitors
None of the NO donors or NOS inhibitors per se (i.e. applied
without simultaneous addition of 5-HT) had an effect on the light production
of M. norvegica, as compared with the saline controls
(Table 2).
NO donors
In all further experiments with NO donors and NOS inhibitors, the
injections of the nitrergic drug were in combination with 5-HT in a solution
producing approximately 0.03 mmol l–1 of 5-HT in the
haemolymph, as in the 5-HT controls. The effects of two NO donors on the
5-HT-stimulated light response were tested. Both SNP and SNAP (0.3 mmol
l–1 in the haemolymph) significantly reduced the total light
production, Ltot, as compared with the 5-HT control
(Fig. 6A). SNAP also reduced
the maximum rate of light production (RLPmax,
Fig. 6B) at the peak of the
response (ip) and delayed the response by prolonging the time to reach the
peak (tip) (Fig.
6C).
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3 mmol l–1 in
the haemolymph) significantly enhanced the response to 5-HT
(Ltot) (Fig.
7A). 3 mmol l–1 L-NAME also delayed
the time to reach the peak of response
(Fig. 7B) and produced a higher
RLPmax compared with the 5-HT control in April
(Fig. 7C). The same kinetic
effects were observed as a response to 0.3 mmol l–1
L-NAME in September. The lowest tested concentration of
L-NAME (0.03 mmol l–1 in the haemolymph) did
not affect any of the parameters (Fig.
7A–C).
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0.3 mmol
l–1 in the haemolymph) together with 5-HT resulted in a
reduced RLPmax of the light response as compared with the
5-HT control. Neither tip nor Ltot was
affected by 8BrcGMP (Fig.
9A-C).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Immunohistochemistry
5-HT
This study shows for the first time that 5-HT-like IR is present and
abundant in the light organs of krill, in nerve fibres terminating at the
sphincter-like structures at the base of the C-cells. The innervation of these
structures by 5-HT fibres agrees with earlier studies using electron and light
microscopy, which describe nerve endings with synaptic vesicles connecting to
C-cells but not to any other cell type in the organ
(Petersson, 1968;
Herring and Locket, 1978). It
is not yet determined whether the `sphincters' are contractile, even though
they consist of filaments that resemble muscle filaments when studied with
electron microscopy (Harvey,
1977; Herring and Locket,
1978). A serotonergic innervation of the sphincter-like
structures, where capillaries empty into the lantern sinus, might suggest that
5-HT can regulate the flow of haemolymph, and thereby the flow of oxygen to
the lantern.
Transmitters may be released not only from the nerve endings, and the
observed 5-HT-IR axons may thus influence other cells and cell functions in
the photophores. This is corroborated by the varicose appearance of these
axons. For example, 5-HT-IR axons follow capillaries between the large
A-cells, which have been described as supportive cells
(Herring and Locket, 1978) but
have also been proposed to be involved in the luminescence reaction
(Bassot, 1966). It is
furthermore possible that released 5-HT diffuses into the haemolymph through
the capillary walls and is transported as a neurohormone to an effector site.
However, a direct stimulation of the photocytes by circulating 5-HT, through
5-HT receptors on the photocytes, is unlikely as isolated photophores do not
respond to 5-HT (Herring and Locket,
1978) (and J.K., personal observations).
NOS
Interestingly, NOS-like IR occurred primarily in non-neuronal structures
associated with capillaries inside the photophores. NO is a potent vasodilator
in mammalian circulatory systems (Bredt and
Snyder, 1992; Bredt and Snyder,
1994; Torilles,
2001) and relaxes smooth muscle in general in both vertebrates and
invertebrates (Olsson and Holmgren,
1996; Elphick and Melarange,
1998). However, the open circulatory system of crustaceans usually
lacks contractile vessels (Wilkens,
1997; Wilkens,
1999). Instead, in some species, the distribution of haemolymph
can be regulated by muscular valves positioned, for example, at the exit of
arteries from the heart or at major branching points of arteries in the
periphery of the circulatory system
(Davidson et al., 1998;
McMahon, 2001).
The sphincter-like structures at the base of the C-cells provide a similar opportunity for the regulation of haemolymph flow. The presence of NOS-like material in the area around these `sphincters' may indicate that NO is involved in the regulation of haemolymph supply to the lantern (as speculated for serotonin, above). This may lead to a modulated oxygen supply and a change in the pH, both of which may affect light production (see below).
NOS-like IR was also seen along the capillaries in the periphery of the
light organ and beside the lens, where the entry point for the photophore
arteries and the ring vessel circling the lens are located. As these parts of
the vessels are not believed to be contractile, this may suggest that NO has
additional functions (Herring and Locket,
1978). NO might be produced along the vessels, released to the
haemolymph and transported bound to haemocyanin
(Jacklet and Koh, 2001). NO
bound to haemocyanin will reduce the oxygen-binding capacity of the
haemocyanin, and thereby decrease the oxygen level in the lantern, and thus
quench the light reaction. NO has furthermore been shown to alter the
excitability of some cell types. In skeletal muscle from the isopod Idotea
baltica, NO stimulates outward potassium currents from the muscle cells,
resulting in a hyperpolarization of the cell
(Hermann and Erxleben, 2001).
Hyperpolarization of the photocytes by NO in the haemolymph would result in
less responsiveness to excitatory stimuli and consequently less light
production.
Pharmacology
5-HT
Several authors have shown that 5-HT stimulates light production in krill
(Kay, 1962;
Kay, 1965;
Doyle, 1966;
Fregin and Wiese, 2002). This
was confirmed in the present study. In addition, we report a possible seasonal
variation in the response to 5-HT, mainly expressed in a few specimens as a
remarkably high response to 5-HT in April and June. In the mouse brain,
seasonal and diurnal changes in sensitivity to serotonin have been correlated
to corresponding changes in the uptake, release and number of binding sites
for serotonin (Rovescalli et al.,
1989; Weiner et al.,
1992). Seasonal fluctuations in krill bioluminesence and the
behavioural implications have been reported and discussed in the literature
(Mauchline, 1960), but the
physiological mechanisms underlying this variation have not been investigated.
The high response to 5-HT in some specimens sampled in April and June in the
present study may be connected to the elevated levels of ambient light in the
spring and summer.
Another possibility is that a particular social behaviour during this
season [i.e. mating, which will start in March in the Gullmar fjord krill
population (Thomasson, 2003)]
involves increased light production in krill. Some specimens may be in a
different physiological state, causing an elevated sensitivity. However
tempting it is to suggest that the variability is caused by mating behaviour,
no obvious correlation with sex or size could explain the sensitivity to 5-HT
in the very highly responsive individuals in this study (J.K., personal
observations).
NO donors
In contrast to the stimulating effect of NO in fireflies
(Trimmer et al., 2001), both
NO donors (SNP and SNAP) used in this study suppressed the total amount of
light (Ltot) produced after stimulation with 5-HT. This
may be compared to the effect of NO in hatchetfish, which is predominantly
inhibitory on adrenaline-induced light production. However, the stimulatory
effect of NO observed in weakly luminescing hatchetfish was never observed in
krill (Krönström et al.,
2005).
The two NO donors affected the kinetic parameters, tip
and RLPmax, differently. SNAP delayed the 5-HT response
significantly, whereas SNP did not. This dissimilarity might be because of the
different chemical composition of SNP and SNAP and different modes of
generation of NO in the tissue. The degradation of SNAP can be catalysed by
membrane components, whereas SNP generates NO mainly in the medium
(Kowaluk and Fung, 1990;
Ohta et al., 1997).
NOS inhibitors
In krill, the average Ltot is higher for individuals
injected with both 5-HT and the NOS inhibitor L-NAME, compared with
5-HT controls. The fact that L-NAME (3 mmol l–1)
enhanced the effect of 5-HT indicates a nitrergic suppressing tonus on light
production. Lower concentrations of L-NAME gave inconclusive
results. There is a large individual variation in the response to the 5-HT and
L-NAME treatment. This may indicate that NO is only produced in
certain situations and that the specimens we have tested could be in different
physiological states.
Taken together, the effects of NO donors and NO blockade support the idea that total light production is reduced by NO. However, the longer tip and lower RLPmax after L-NAME treatment as well as after treatment with NO donors appear contradictory. The effects cannot be explained by a simple model for an inhibitory control by NO, but suggest that several interacting inhibitory as well as excitatory mechanisms are involved in the normal control of light production and are affected by the NO tonus in the preparation.
cGMP
In some crustacean tissues the effects of NO are mediated through
stimulation of cGMP production. This is shown pharmacologically in
preparations from the abdominal nervous system of the crayfish
Pacifastacus leniusculus (Aonuma
and Newland, 2002). Moreover, cGMP IR is elevated after NO
stimulation of certain cells in the cardiac ganglion of the crab Cancer
productus, and in the abdominal nervous system of the crayfish
Procambarus clarcii (Aonuma,
2002). In contrast, NO does not affect luminescence through the
cGMP pathway in fireflies and hatchetfish, two species in which NO has been
demonstrated to be involved in the regulation of light production. The action
of NO in these systems instead seems to be linked to mitochondrial respiration
(Trimmer et al., 2001;
Krönström et al.,
2005). Similarly, in the present study, injections of a
membrane-permeable analogue of cGMP did not mimic the effect of the NO donors,
suggesting that the inhibitory effect of NO on the total light production does
not involve cGMP formation. This is further supported by the lack of effect of
the cGMP-antagonist ODQ. However, the effect of the analogue on
RLPmax is contradictory, and again implies the involvement
of several mechanisms. It also remains to be established as to what extent and
how the light reaction in krill is dependent on cellular respiration.
In conclusion, the results from this study indicate that NO has a role, or several roles, in the control of bioluminescence in krill. NO could possibly restrict the supply of oxygen to the photocytes, or act directly on photocytes or photocyte-controlling nerves inside the photophore. The inhibitory effects of NO on krill photophores differ from the stimulatory effects of NO on firefly and the dual effects on hatchetfish light production. This highlights the diversity of bioluminescent systems as well as the multiplicity of physiological systems in which NO is involved.
Abbreviations
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Acknowledgments |
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References |
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