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First published online June 29, 2006
Journal of Experimental Biology 209, 2804-2810 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02309
Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis
Department of Zoology, Oregon State University, Corvallis, OR 97331, USA
* Author for correspondence (e-mail: perezs{at}science.oregonstate.edu)
Accepted 3 May 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: Aiptasia pallida, nitric oxide, peroxynitrite, oxidative stress, Symbiodinium, zooxanthellae, coral bleaching, Cnidaria, dinoflagellate, innate immunity, programmed cell death, necrosis, apoptosis, symbiosis
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Glynn and D'Croz, 1990). This
process, known as coral (cnidarian) bleaching, is often lethal to the host and
can have devastating ecological effects on the coral reef ecosystem
(Glynn, 1996;
Hoegh-Guldberg, 1999). In
cnidarian-dinoflagellate symbioses, exposure to elevated temperature can
result in inhibition of algal photosynthesis and increased production of
reactive oxygen species (ROS) such as superoxide radical
(Franklin, 2004;
Lesser, 1996;
Lesser et al., 1990;
Perez et al., 2001). The
increase in ROS production is hypothesized to increase cellular damage and
lead to bleaching; however, the cellular and molecular mechanisms leading to
the loss of algae is poorly understood.
Cnidarian bleaching is known to be mediated in part through apoptosis and
necrosis leading to the loss of integrity of gastrodermal tissue that contains
the algae (Dunn et al., 2004).
However, the events that lead to host cell death have not been studied in
detail. In other systems, an important mediator of cell death due to oxidative
stress is the reactive nitrogen species peroxynitrite, which is a reaction
product of superoxide and nitric oxide (NO)
(Radi et al., 2000). In
animals, NO is produced by a family of enzymes known as nitric oxide synthases
(NOS; EC 1.14.13.39). These enzymes catalyze the conversion of arginine, NADPH
and O2 to NO, citrulline and NADP+. Early evidence
suggests that NO is produced in symbiotic cnidarians and that it may play a
role in bleaching. In the symbiotic anemone Aiptasia pallida, an
arginine-dependent NOS-like activity has been reported
(Trapido-Rosenthal et al.,
2001). Further, NO was produced in freshly isolated algae from the
coral Madracis mirabilis and was implicated in the bleaching process
(Trapido-Rosenthal et al.,
2005).
We were interested, therefore, in further investigation of NO in symbiotic
cnidarians and its potential cellular role in the bleaching process. We
visualized production of NO in vivo as a function of heat stress in
the symbiotic anemone Aiptasia pallida, using laser scanning confocal
microscopy and the NOsensitive fluorescent dye DAF-FM
(Nagano and Yoshimura, 2002).
We present evidence in support of a model in which the host cell increases its
production of NO as a function of an increased oxidative load during exposure
to elevated temperatures. We suggest that this constitutes a cytotoxic
response that leads to bleaching.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) and kept in the dark. Algae from the Florida anemones
(Symbiodinium sp.) were isolated by homogenizing anemones in a glass
tissue grinder followed by repeated centrifugations and subsequent
resuspension in sterile seawater. The algae were then placed in 50 ml tubes
with sterile Guillard's f/2 enriched seawater culture medium (Sigma, St Louis,
MO, USA). Algal cultures were kept in the same light and temperature
conditions as the symbiotic anemones.
Confocal microscopy
For preparation for confocal microscopy, the media of experimental anemones
was replaced with relaxing solution of a 1:1 ratio of 37 mmol l-1
MgCl2:seawater (35
) with 3 µl ml-1 of the NO
probe DAF-FM-DA (Molecular Probes, Eugene, OR, USA)
(Nagano and Yoshimura, 2002).
After incubating the anemones for at least 30 min in the dark, the media was
removed and a few drops of melted 1% low-melting agarose in relaxing solution
cooled to 30°C was added to immobilize the anemones. After allowing the
agarose to gel for 1 min, 3 ml of relaxing media was added on top of the
agaroseembedded anemones. Unstained control anemones were processed as above
without adding the probe to the mix. These were used to control for possible
host tissue autofluorescence. Cultured algae were processed by incubating 1 ml
of suspension with 1 µl ml-1 DAF-FM-DA for at least 30 min
before observing on a glass slide and cover slip. The samples were observed
under a Zeiss LSM510 Meta microscope (The Center for Genome Research and
Biocomputing at Oregon State University) with a 40x/0.8 3.2 mm working
distance water objective lens. Excitation was provided by an argon laser at
488 nm to excite the DAF-FM probe and a HeNe543 laser to excite chlorophyll
autofluorescence. DAF-FM NOdependent fluorescence was detected using a 510-530
nm filter and chlorophyll autofluorescence using the metadetector at 600-700
nm. Each excitation wavelength (488 and 543 nm) was used separately on
different scans using the multiscan function. Before image scanning, the focal
plane of the optical section was adjusted to include the gastrodermal layer of
tentacles. All images were obtained with the same software scanning settings
including detector gain and laser intensity settings. After visualization,
samples that showed no NOdependent fluorescence were subsequently incubated
for 30 min in the NO donor sodium nitroprusside (1 mmol l-1 SNP;
Sigma, St Louis, MO, USA), and fluorescence was measured to confirm successful
loading of the dye. Quantification of NO-dependent DAF-FM fluorescence was
achieved by first defining the gastrodermal portions as regions of interest
and measuring the average pixel intensity value for that region with the LSM 5
software.
Experiments
To test the effect of heat stress on NO production, 3-5 small aposymbiotic
and symbiotic anemones (5-10 mm long) were each placed in 3 ml of artificial
seawater in 5 ml Petri dishes. The Petri dishes were modified by fitting them
with a glass cover slip adhered to a hole drilled on the bottom. The anemones
were pre-incubated overnight at 25°C. After the preincubation, the
anemones were incubated in either 25°C or 33°C for 24 h on a 12 h:12 h
light:dark photoperiod. Algal cultures (50 ml) were similarly heat stressed.
After the incubation, the anemones and algal cultures were processed for
confocal microscopy. To examine the effect of an NOS inhibitor on NO
production after heat stress, heat-stressed or control symbiotic anemones were
incubated for 10 min in l0 mmol l-1 L-aminoguanidine
(LAG; Sigma) before processing for confocal microscopy. Aposymbiotic anemones
that served as a positive control for host NOS activity were incubated for 5 h
in 1 µg ml-1 lipopolysaccharide (LPS; Sigma) before preparation
for confocal microscopy. Some LPS-treated anemones were also pre-incubated in
LAG as above.
To test the effect of 3-(3',4'-dichlorphenyl)-1,1-dimethylurea (DCMU; Sigma) on NO production, anemones or cultured algae were incubated in 50 µmol l-1 DCMU for 24 h. Samples were then prepared for confocal microscopy.
Bleaching experiments were carried out by incubating medium-sized (0.5-1 cm
oral disc diameter) symbiotic anemones at 25°C with 1.0 mmol
l-1 SNP with or without 1 mmol l-1 of the NO scavenger
2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO;
Sigma) or at 33°C with or without 20 mmol l-1 cPTIO for 24 h.
Controls were included and each anemone was incubated individually in 5 ml
Petri dishes. Bleaching was quantified using methods similar to those
previously published (Perez et al.,
2001). Briefly, both algae expelled into the media from anemones
and those remaining in the host tissues (in hospite algae) were
counted. Percent bleaching was calculated as the number of expelled
algae/(expelled algae + number of in hospite algae). In a separate
experiment, small anemones were either heatstressed with or without 20 mmol
l-1 cPTIO at 33°C for 24 h or incubated with 1.0 mmol
l-1 SNP with or without 20 mmol l-1 cPTIO for 3 h.
Treated anemones as well as control anemones (also with or without 20 mmol
l-1 cPTIO) were then rinsed with seawater and prepared for confocal
microscopy using DAF-FM to measure NO-dependent fluorescence as described
above.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Exposure to elevated temperature resulted in a significant twofold increase in
NOdependent DAF-FM fluorescence in tentacles of symbiotic anemones
(Fig. 1; t-test,
P=0.0015). The fluorescent NO-sensitive signal was found largely in
the host gastrodermal cells containing the algae, both in the intact tissue as
well as in the host cells released during bleaching
(Fig. 1A inset). The difference
in the fluorescent signal between control and heatstressed anemones was not
due to unequal loading of the dye as a function of temperature treatment since
addition of exogenous NO to controls, by incubation with the NO donor sodium
nitroprusside (SNP), always resulted in an increase of the NO-dependent
fluorescent signal (data not shown). Unstained controls did not show
autofluorescence of host tissues.
|
The host A. pallida as a source of NO during heat stress
To examine more closely the source of NO during exposure to elevated
temperature, we performed the heat stress experiments on aposymbiotic anemones
and cultured Symbiodinium from A. pallida loaded with
DAF-FM. We did not observe NO production in either aposymbiotic animals or
cultured algae in isolation as a function of heat stress. This suggests that
the partners in combination are required to cause the production of NO.
|
). To induce NOS-like activity in anemones, we incubated
aposymbiotic anemones in LPS (1 µg ml-1), which is known to
cause the upregulation of inducible NOS in vertebrate systems
(Ganster and Geller, 2000). LPS
induced NO production in gastrodermal tissues of aposymbiotic A.
pallida at similar levels to those observed in heat-stressed symbiotic
anemones (Fig. 2A). Incubating
LPS-treated anemones with LAG (10 mmol l-1) resulted in strong
inhibition of NO production (Fig.
2A). To test whether the heat-stress-induced NO production
observed in symbiotic anemones was due to a host NOS inhibitable by LAG, we
incubated heat-stressed anemones in 10 mmol l-1 LAG and measured NO
production. Incubation of heat-stressed symbiotic anemones in the NOS
inhibitor also significantly inhibited NO production due to heat stress
(Fig. 2B; ANOVA,
P=0.006; Tukey HSD, P=0.021). This suggests that in response
to exposure to elevated temperature, symbiotic anemones produce NO through a
hostregulated NOS-like activity.
Oxidative stress can trigger the production of NO in symbiotic anemones
In vertebrate systems, oxidative stress is another wellknown signal for the
upregulation of inducible NOS (Mendes et
al., 2003). We hypothesized that production of ROS by the algae, a
phenomenon known to occur during heat stress, would result in NO production.
To test for NO production due to elevated oxidative stress, we incubated
symbiotic and aposymbiotic anemones as well as cultured algae in DCMU, an
inhibitor of photosynthetic electron transport known to increase production of
ROS and trigger bleaching (Franklin et al.,
2004; Lesser,
1996). Incubating symbiotic anemones with 50 µmol
l-1 DCMU elicited a nearly threefold increase in NO production in
tentacles similar to that seen in heat-stressed anemones while DCMU did not
have a significant effect in aposymbiotic anemones
(Fig. 3; t-test,
P=0.0041). Further, we could not detect production of NO in cultured
algae in the presence of DCMU (data not shown). These results suggest that
anemones produce NO in response to conditions known to elicit oxidative stress
in the algae.
|
Nitric oxide induces cnidarian bleaching in A. pallida
To test whether NO plays a role in bleaching, we incubated anemones with
the NO donor SNP at room temperature and measured the release of algae from
host tissues. SNP-derived NO caused a significant increase in bleaching,
increasing from less than 1% in controls to 17% at 1 mmol l-1 SNP
(Fig. 4A; t-test,
P=0.012). Further, the effect of SNP on bleaching was significantly
decreased by co-incubation with the NO scavenger cPTIO
(Fig. 4A; t-test,
P=0.0368). In addition, incubating anemones in 20 mmol l-1
cPTIO during exposure to elevated temperature (33°C) significantly
decreased bleaching by 50% (Fig.
4B; t-test P=0.0176). The NO-dependent DAF-FM
fluorescence significantly increased in anemones incubated with 1 mmol
l-1 SNP as well as anemones exposed to elevated temperature
(Fig. 4C; two-way ANOVA,
P<0.001; Tukey HSD, P<0.05). Co-incubation of both SNP
and heat-stressed anemones with 20 mmol l-1 cPTIO effectively
decreased NOdependent DAF-FM fluorescence to levels found in control anemones
(Fig. 4C; two-way ANOVA,
P<0.001; Tukey HSD, P<0.05).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Symbiotic anemones exposed to elevated temperatures produced NO while
aposymbiotic anemones do not. There are two possible (but not mutually
exclusive) explanations for this result. Either symbiotic algae in the host
are responsible for the production of NO or the host produces NO in response
to heatstressed algae. There are several lines of evidence that support the
second scenario. First, we did not detect any production of NO in cultured
algae exposed to elevated temperatures. The algae, however, could be producing
NO during heat stress only during symbiosis, perhaps in response to an unknown
hostderived factor. But, to date, no homologous NOS-encoding genes or cDNAs
have been discovered in plants or lower eukaryotes including apicomplexans, a
sister taxon to dinoflagellates (Chandok et
al., 2003; Gardner et al.,
2002; Guo et al.,
2003). It is possible that NO could be produced by NOSindependent
mechanisms such as by the enzyme nitrate reductase, as has been shown in the
chlorophyte Chlamydomonas
(Sakihama et al., 2002). If
the symbionts are producing NO through an NOS-independent activity, then using
a classic NOS inhibitor such as LAG should not inhibit NO production of
heat-stressed symbiotic anemones. However, we were able to drastically inhibit
NO production with LAG at concentrations that also inhibited LPS-induced NO
production in aposymbiotic anemones (Fig.
2). In other systems, LPS has been demonstrated to induce the
upregulation of the inducible form of NOS (iNOS) transcription through nuclear
factor 
B (NFB)-dependent signaling as part of the inflammatory
response of mammalian phagocytes in response to bacterial pathogens
(Ganster and Geller, 2000).
This pathway has not been described in cnidarians. In a recent publication,
preparations of expelled as well as freshly isolated algae from the coral
Madracis mirabilis showed increased NOS activity during heat stress,
as measured by the conversion of arginine to citrulline
(Trapido-Rosenthal et al.,
2005). This apparently algal NOS-like activity may be explained by
host cell contamination that, in our experience, is unavoidable in such
preparations. Expelled material during bleaching also typically contains
numerous gastrodermal cells containing algae
(Gates et al., 1992), which we
have observed to produce NO as well (Fig.
1A inset). Taken together, this evidence suggests that the host is
responding to heat-stressed algae by producing NO.
Heat stress inhibits photosynthesis while stimulating ROS production in the
algae (Lesser, 1996). Inducing
oxidative stress in the algae by blocking the electron transfer from
photosystem II with the use of DCMU
(Franklin et al., 2004;
Lesser, 1996) also led to the
production of NO in symbiotic anemones only but not in cultured algae or
aposymbiotic anemones. Like LPS, oxidative stress is known to lead to
upregulation of iNOS through the activation of the transcription factor
NFB (Mendes et al.,
2003). Interestingly, Plasmodium berghei, an apicomplexan
parasite (a sister taxon of dinoflagellates), induces a similar response of
upregulation of NOS and oxidative stress, leading to host cell death, when it
infects the epithelial cells of the host mosquito Anopheles stephensi
(Kumar et al., 2004). We
therefore hypothesize that ROS is acting as a signal to induce the host cell
production of NO during heat stress in symbiotic A. pallida
(Fig. 5).
|
).
Incubating anemones with the NO donor SNP resulted in bleaching while
co-incubation with the NO scavenger cPTIO decreased the rate of bleaching in
both heatstressed anemones and anemones incubated in SNP. Production of NO
during heat stress was assayed after 24 h of exposure to elevated
temperatures, but it is likely that production of NO began at an earlier time
point after stress to elicit bleaching, given that symbiotic A.
pallida had already expelled algae within 24 h of exposure to elevated
temperatures. We hypothesize that the production of NO could have deleterious
effects in conjunction with increased oxidative stress brought about by the
effect of elevated temperature on the photosynthetic apparatus of the
algae.
NO can react with superoxide to form the reactive nitrogen species
peroxynitrite (ONOO-), which can act in several deleterious ways.
It can (1) undergo decomposition reactions to produce the highly reactive
hydroxyl radical (Beckman et al.,
1990; Radi et al.,
2000); (2) inactivate several steps in the mitochondrial electron
transport chain and ATP synthesis, thereby increasing the production of ROS
(Radi et al., 2000); (3)
inactivate Mn-SOD, leading to a rise in the steady-state levels of ROS and (4)
influence homeostasis by increasing the permeability of the mitochondrial
membrane (Radi et al., 2000).
This last mechanism is critical since it is known to cause the release of
potent pro-apoptotic molecules such as cytochrome c from
mitochondria. We hypothesize that the negative effect of high levels of NO
during bleaching is in part due to its conversion to cytotoxic peroxynitrite
concomitant with the increase in oxidative stress
(Fig. 5).
Some coral-alga associations are more tolerant of hyperthermic bleaching
than others (Fitt and Warner,
1995). The observed differences in tolerance to elevated
temperature may result from the differential tolerance of the algal strain
(phylotype) present (Buddemeier and Fautin,
1993; Perez et al.,
2001; Rowan et al.,
1997). Since we do not fully understand the bleaching mechanism,
we also do not know how the differential susceptibility of the algae
translates mechanistically into differential bleaching. Could differential
host production of NO in response to differences in the algal tolerance
explain this variation in bleaching? Based on our model, we hypothesize that
the differential susceptibility to heat stress of algal photosynthesis also
leads to differential levels of oxidative stress and therefore triggers
differential production of NO by the host.
The results of this study show that, upon exposure to elevated temperature,
symbiotic A. pallida produce NO through an NOS-like system and that
this process leads to bleaching. We propose that bleaching is an innate animal
response to algal dysfunction that, in turn, has been linked to temperature
stress. This response is similar to that described in some mammalian systems
exposed to pathogens together with oxidative stress and therefore suggests
that there is a remarkable degree of conservation of these cellular processes.
The cytotoxic effect of NO during bleaching is likely dependent in part on the
levels of oxidative stress and the production of damaging reactive nitrogen
species such as peroxynitrite (Fig.
5). This hypothesized detrimental interaction between NO and
superoxide provides additional insight into the well-described importance of
the superoxidedetoxifying enzyme superoxide dismutase in cnidarian-alga
symbioses (Richier et al.,
2005; Richier et al.,
2003).
Another example of conservation of cellular mechanisms that spans large
taxonomic distances is the production of NO in A. pallida upon
exposure to LPS. This mechanism may explain bleaching in corals exposed to
Vibrio sp. and bacterial SOD as a virulence factor in that process
(Ben-Haim et al., 2003). The
regulatory role of NO as a function of oxidative stress may also explain some
of the bleaching variability observed in both the laboratory and the field
linked to the differential tolerance of algal photosynthesis to elevated
temperatures. Nitric oxide is emerging as an important regulator in both
parasitic and mutualistic symbioses and this illustrates the importance of
understanding the innate immune response mediating host-symbiont interactions
in these systems.
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Acknowledgments |
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