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First published online August 8, 2008
Journal of Experimental Biology 211, 2617-2623 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019729
Redox regulation of mitochondrial sulfide oxidation in the lugworm, Arenicola marina
Institut für Zoophysiologie, Heinrich-Heine-Universität, 40225 Düsseldorf, Germany
* Author for correspondence (e-mail: Tatjana.Hildebrandt{at}uni-duesseldorf.de)
Accepted 15 June 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: redox regulation, sulfide oxidation, Arenicola marina, alternative oxidase, ATP production, glutathione, ascorbate, dehydroascorbate
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Grieshaber and Völkel,
1998). This species is highly tolerant towards both stress factors
and is therefore often used to study the underlying adaptational strategies.
The mitochondria of the body wall musculature are the main site of sulfide
oxidation in A. marina, producing thiosulfate as the dominant aerobic
end product that is excreted into the seawater
(Völkel and Grieshaber,
1994; Hauschild et al.,
1999).
The first step in mitochondrial sulfide oxidation is presumably catalyzed
by a sulfide:quinone oxidoreductase (SQR) bound to the inner mitochondrial
membrane. The SQR oxidizes sulfide to persulfides and transfers the electrons
to the ubiquinone pool (Theissen and
Martin, 2008). Thus, H2S can be used as a respiratory
substrate to drive ATP synthesis
(Völkel and Grieshaber,
1997). A putative sulfur dioxygenase and a sulfurtransferase in
the mitochondrial matrix convert the persulfides, produced by the SQR, to
thiosulfate (Hildebrandt and Grieshaber,
2008).
In isolated mitochondria, the energy-conserving sulfide oxidation pathway
via cytochrome oxidase is inhibited by sulfide concentrations
exceeding 10 µmoll–1. At higher sulfide concentrations,
the electrons are transferred to oxygen via an alternative terminal
oxidase (AOX), presumably resembling the enzyme found in plant mitochondria as
it is equally cyanide insensitive and also inhibited by salicylhydroxamic acid
(SHAM) (Völkel and Grieshaber,
1996). A DNA sequence similar to the plant AOX has been detected
in some invertebrates such as Crassostrea gigas, but the function of
the respective gene product remains to be proven
(McDonald and Vanlerberghe,
2004).
The position of the AOX in the respiratory chain is unknown, and different
studies have demonstrated varying rates of mitochondrial sulfide oxidation in
A. marina (Völkel and
Grieshaber, 1994; Völkel
and Grieshaber, 1996;
Völkel and Grieshaber,
1997). Sulfide detoxification capacities apparently change with
the season, as does the redox environment of the lugworm tissue
(Völkel and Grieshaber,
1994; Keller et al.,
2004). Therefore, the redox state of the cell may take part in the
regulation of mitochondrial sulfide oxidation.
In the present study, we demonstrate that reduced glutathione (GSH) and
ascorbate, which are both major cellular antioxidants
(Wu et al., 2004;
Linster and Van Schaftingen,
2007), as well as the oxidized form of vitamin C, dehydroascorbate
(DHA), are able to selectively activate the detoxifying and the
energy-conserving sulfide oxidation pathways in isolated mitochondria.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) without sediment in darkened and aerated tanks for up to two
weeks.
Purification procedures
A mitochondrially enriched particulate fraction was prepared from the body
wall musculature of A. marina, as described in Völkel and
Grieshaber (Völkel and Grieshaber,
1997).
Assay of mitochondrial respiration
Mitochondrial oxygen consumption (nmol O2 mg
protein–1 min–1) was measured
polarographically in an oxygraph respirometer (Oroboros; Innsbruck, Austria)
at 15°C. The reaction mixture (2 ml) contained incubation medium (450
mmoll–1 glycine, 250 mmoll–1 sucrose, 20
mmoll–1 Tris, 1 mmoll–1 EGTA, 0.2% BSA
(fatty acid free), 5 mmoll–1 K2HPO4, 3
mmoll–1 MgCl2 and 100 mmoll–1
KCl, pH 7.5) and 0.1–0.7 mg ml–1 of mitochondrial
protein. In order to calculate the mitochondrial respiratory rates, the
incubation medium was assumed to contain 269 µmoll–1
O2 at air saturation
(Reynafarje et al., 1985).
Malate (8 mmoll–1), succinate (4 mmoll–1), or sulfide (5–100 µmoll–1) was added as a respiratory substrate either in the presence of 1 mmoll–1 ADP (state 3 respiration) or without ADP (state 4 respiration). The respiratory control ratios (RCRs) were determined by dividing the state 3 by the state 4 respiration rate. For inhibitor studies, 2–10 µl of the respective stock solution was added to the assay, resulting in a final concentration of 5 µmoll–1 myxothiazole, 0.05 mmoll–1 KCN, 1 mmoll–1 NaN3 or 0.5 mmoll–1 SHAM. KCN and NaN3 were dissolved in distilled water, SHAM was dissolved in dimethylsulfoxide, and myxothiazole was dissolved in ethanol. The solvents did not influence mitochondrial sulfide oxidation in the concentrations applied. To evaluate the effect of the cellular redox state on mitochondrial sulfide oxidation, either 2.5 mmoll–1 GSH + 2.5 mmoll–1 ascorbate or 1 mmoll–1 dehydroascorbate (DHA) was added to the assay prior to the sulfide injections. As KCN reacts with DHA, NaN3 was used to inhibit cytochrome oxidase in DHA containing assays.
The oxygen affinities of the terminal oxidases were determined according to
Gnaiger et al. (Gnaiger et al.,
1995). Mitochondria were allowed to completely consume the oxygen
contained in the respiration medium, and the oxygen concentration was recorded
at one-second intervals. Signal corrections were applied using DatLab 2.1
(Oroboros) to account for the time response of the polarographic oxygen
sensor, as well as for the oxygen leak and blank oxygen consumption. Oxygen
consumption rates were calculated from the corrected signal and plotted
against the oxygen concentration. Km
(Michaelis–Menten constant) values were calculated by non-linear
least-square analysis of the data fitted to the Michaelis–Menten
equation using the enzyme kinetics module of SigmaPlot version 9.01 (Systat
Software; Erkrath, Germany). Data are given as means ± standard
deviation of the results from three independent experiments. Cytochrome
oxidase was analysed using malate (8 mmoll–1) as a substrate
in the presence of 1 mmoll–1 ADP and 0.5
mmoll–1 SHAM. The energy-conserving and the detoxifying
sulfide oxidation pathways were activated by 1 mmoll–1 DHA or
2.5 mmoll–1 GSH + 2.5 mmoll–1 ascorbate,
respectively.
Measurements of ATP production
ATP production was determined using a coupled enzyme assay
(Powell and Somero, 1986), as
described in detail by Bagarinao and Vetter
(Bagarinao and Vetter, 1990).
The reaction mixture (1 ml) contained 10 mmoll–1 glucose, 3.5
U ml–1 hexokinase, 1.75 U ml–1
glucose-6-phosphate dehydrogenase, 0.5 mmoll–1
NADP+, 50 µmoll–1 ADP, 20
µmoll–1
P1,P5-di(adenosine-5')pentaphosphate and
40–200µg ml–1 mitochondrial protein in the
incubation medium. Assays were performed in duplicate at 15°C. The
reaction was started by the addition of sulfide (5–100
µmoll–1). Inhibitors and activators were applied at the
same concentrations as for respiratory studies. The ATP/S ratio was determined
by calculating the total concentration of ATP produced after 5
µmoll–1 sulfide had been completely consumed, which was
verified by high performance liquid chromatography (HPLC) (see below).
Controls were performed using heat-inactivated mitochondria (30 min at 85°C).
Substrate solutions
Sulfide stock solutions (1–10 mmoll–1) were prepared
in deoxygenated distilled water immediately before use in assays. The sulfide
concentration was analysed photometrically using a commercial sulfide test
based on Methylene Blue production (Spektroquant; Merck, Darmstadt, Germany).
Samples were fixed with 50mmoll–1 zinc acetate in
150mmoll–1 NaOH prior to analysis.
Determination of sulfur compounds
The concentrations of sulfide and thiosulfate in the mitochondrial
suspensions were determined using the monobromobimane HPLC method, as
described in Völkel and Grieshaber
(Völkel and Grieshaber,
1994).
Determination of ascorbate
Samples were stabilized by adding the same volume of 0.1
moll–1 perchloric acid. The ascorbate concentration was
analysed by HPLC (Reiber et al.,
1993).
Statistical analyses
Data are given as means ± standard deviation of the results from 3
to 12 different preparations, each comprising approximately 10–15
animals. Significant differences between means were evaluated by
t-tests at the P<0.05 level using a statistical software
package (SigmaStat version 3.1, Systat Software).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In the absence of any activator, maximal rates of state 3 oxygen consumption and ATP production were achieved with 5–10µmoll–1 sulfide (RCR=2.44±0.58), with both rates decreasing with increasing sulfide concentration (Fig. 1A). During complete oxidation of 5µmoll–1 sulfide, mitochondria produced 7.50±0.84µmoll–1 ATP, corresponding to a ratio of 1.50±0.17 molecules of ATP produced per molecule of H2S consumed. Sulfide-induced oxygen consumption was partially inhibited by either myxothiazole, SHAM or KCN. By contrast, ATP production was completely blocked by myxothiazole or KCN but was insensitive to SHAM (Fig. 1D).
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In the presence of DHA, oxygen consumption rates were stimulated by the addition of ADP even at high sulfide concentrations; orginal recordings are depicted in Fig. 2A (trace 2) for 50µmoll–1 sulfide. State 3 and state 4 respiratory rates were constant when up to 100µmoll–1 sulfide was added as a substrate (Fig. 1C), resulting in an RCR of 2.07±0.18. Accordingly, the lugworm mitochondria produced ATP during sulfide oxidation in the presence of DHA (Fig. 1C and Fig. 2B). Rates of state 3 respiration and ATP production were significantly increased by DHA at sulfide concentrations exceeding 10 µmoll–1. Both rates were equally inhibited by myxothiazole and NaN3 but were hardly affected by SHAM (Fig. 1F). DHA changed neither the oxygen content nor the ATP concentration in the assay when added separately. To prove whether DHA acted as an electron acceptor for sulfide oxidation, the concentrations of possible substrates and products were determined. During complete oxidation of 100µmoll–1 sulfide in the presence of 1mmoll–1 DHA, 44.52±2.56µmoll–1 thiosulfate accumulated in the mitochondrial suspension and 93.53±7.87µmoll–1 O2 was consumed whereas only 1.1±0.7µmoll–1 ascorbate was detectable.
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GSH and ascorbate significantly increased sulfide-induced oxygen
consumption rates at high sulfide concentrations (
20
µmoll–1; Fig.
1B). However, respiratory rates were not stimulated by the
addition of ADP, and the mitochondria produced significantly less ATP during
sulfide oxidation than without GSH and ascorbate. Oxygen consumption was
insensitive towards myxothiazole and cyanide but was completely inhibited by
SHAM (Fig. 1E). A similar
effect was achieved with either GSH or ascorbate added separately; however,
oxygen consumption rates were maximal and remained constant until the sulfide
added had been completely consumed, only if both reductants were present.
Glutathione disulfide (GSSG), the oxidized form of glutathione, had no effect
on mitochondrial sulfide oxidation rates.
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Similarly, 50 µmoll–1 sulfide normally inhibited succinate respiration by 85±3% (Fig. 4A). In the presence of GSH, rates of succinate respiration were not changed but could be stimulated by adding sulfide (Fig. 4B). NaN3 completely inhibited succinate respiration whereas GSH-activated sulfide oxidation was not affected (Fig. 4C).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Thus, sulfide-adapted animals have had to
evolve mechanisms to effectively exploit H2S while simultaneously
avoiding poisoning. A branched respiratory chain enables A. marina to
use H2S as a respiratory substrate or switch to a pathway of rapid
sulfide detoxification, which is independent of the ATP demand
(Völkel and Grieshaber,
1996; Völkel and
Grieshaber, 1997). Selective activators of the energy-conserving
and the detoxifying sulfide oxidation pathways in lugworm mitochondria have
been identified.
Detoxification of H2S
An alternative terminal oxidase similar to the extensively characterized
plant AOX has been postulated for some intertidal sulfide-adapted
invertebrates such as A. marina and the ribbed mussel Geukensia
demissa (Völkel and Grieshaber,
1996; Kraus and Doeller,
2004). The AOX of plant mitochondria is non-protonmotive and
couples the oxidation of ubiquinol to the reduction of oxygen to water
(Vanlerberghe and McIntosh,
1997). It contains a non-haem di-iron center but no cytochromes
and is therefore cyanide, as well as sulfide, resistant
(Azcon-Bieto et al., 1989;
Siedow et al., 1995).
In isolated lugworm mitochondria, the electron flow during sulfide
oxidation splits between the classical respiratory chain and the AOX pathway,
since oxygen consumption was decreased but not completely stopped by the
addition of each of the inhibitors of complex III, complex IV and the AOX. The
ROS scavengers, GSH and ascorbate, selectively activated the detoxifying
sulfide oxidation pathway (Fig.
6A). Hardly any ATP was produced during sulfide oxidation in the
presence of GSH and ascorbate. Thus, the proton translocating complexes III
and IV of the respiratory chain were not involved, and sulfide oxidation
via the AOX was insensitive towards myxothiazole, NaN3 and
cyanide, which are potent inhibitors of these enzymes. When using KCN in
assays containing reactive sulfur intermediates, possible side reactions have
to be taken into account. In lugworm mitochondria, cyanide may act as a
persulfide acceptor for the SQR and pull the reaction towards sulfide
oxidation (Theissen and Martin,
2008). Nevertheless, as KCN completely inhibited sulfide-induced
ATP production, the main respiratory chain was definitely blocked. The
equivalent oxygen consumption rates during sulfide oxidation with either
myxothiazole or cyanide added as an inhibitor further demonstrate that the AOX
pathway can be stimulated irrespective of the further fate of the immediate
sulfide oxidation product. The present results therefore clearly demonstrate
that lugworm AOX either accepts the electrons directly from the SQR or is fed
by the ubiquinone pool.
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ATP production from H2S
Not only sulfide-tolerant animals but also chicken liver mitochondria use
sulfide as a substrate for oxidative phosphorylation; indirectly, it has also
been demonstrated for human cells (Powell
and Somero, 1986; Bagarinao and
Vetter, 1990; Völkel and
Grieshaber, 1997; Hahlbeck et
al., 2000; Yong and Searcy,
2001; Goubern et al.,
2007). Isolated mitochondria only synthesize ATP in the presence
of low sulfide concentrations; however, the inhibitory concentration of
H2S clearly depends on the cellular environment. The mussel G.
demissa, for example, inhabits sediments that regularly contain
millimolar sulfide concentrations. Pieces of gill tissue oxidize up to
200µmoll–1 with maximal rates, but isolated gill
mitochondria are already inhibited by 8 µmoll–1
H2S (Lee et al.,
1996; Parrino et al.,
2000). The present study demonstrates that lugworm mitochondria
use high sulfide concentrations as a substrate for chemolithotrophic ATP
production in the presence of 1 mmoll–1 DHA
(Fig. 6B).
ATP production in A. marina was SHAM insensitive but was
completely inhibited by myxothiazole, cyanide or NaN3. Therefore,
the electrons from sulfide oxidation are transferred to oxygen via
the respiratory chain complexes III and IV. Six protons are translocated for
each electron pair so that 1.5 molecules of ATP can be produced
(Hinkle, 2005). The SQR
oxidizes H2S to persulfides, corresponding to a two-electron
oxidation (Theissen and Martin,
2008), and an ATP/S ratio of 1.5 was experimentally confirmed for
5 µmoll–1 sulfide. The ATP yield decreases with increasing
sulfide concentrations to 0.9 ATP/S at 8 µmoll–1
H2S and 0.7 ATP/S at 11 µmoll–1 H2S,
probably because a higher percentage of the electrons is transferred to oxygen
via the alternative oxidase
(Völkel and Grieshaber,
1997).
Redox regulation of sulfide oxidation
Reactive oxygen species (ROS) are produced mainly by mitochondria when
electrons leak from a highly reduced respiratory chain
(Andreyev et al., 2005). Apart
from causing oxidative damage to several cellular constituents, ROS also
function as signal molecules (Moran et
al., 2001; Damdimopoulos et
al., 2002).
Protein sulfhydryl groups are crucial to redox regulation as they can be
reversibly oxidized, forming inter- or intra-molecular disulfide bridges
(Ghezzi, 2005). The plant AOX
is a dimer covalently linked by a disulfide bridge that has to be reduced and
form a thiohemiacetal with pyruvate in order to produce the active
conformation (Rhoads et al.,
1998; Vanlerberghe et al.,
1998). Thus, the redox state regulates the partitioning of
electron flux between AOX and cytochrome oxidase in plant mitochondria
(Berthold et al., 2000). The
lugworm AOX may be regulated in a similar way, as the detoxifying sulfide
oxidation pathway was active exclusively under reducing conditions. However,
sulfide but not pyruvate was essential for AOX activity in A.
marina.
GSH and ascorbate are important ROS scavengers and are present in
millimolar concentrations in mammalian cells
(May et al., 1997). In the
body wall tissue of A. marina approximately 0.6
mmoll–1 GSH was detected in the winter
(Buchner et al., 1996) but
there are no data available on the ascorbate concentration or on seasonal
changes of the antioxidant status in the lugworm.
GSH and ascorbate could activate sulfide detoxification by reducing a
regulatory cysteine residue. Furthermore, AOX activity could be reversibly
modulated by glutathionylation. Several mitochondrial proteins form mixed
disulfides with GSSG under resting conditions and are activated by reduction
at a high GSH:GSSG ratio (Brigelius et al.,
1983; O'Donovan and Fernandes,
2000; Ghezzi,
2005).
The finding that the AOX activity in lugworm mitochondria strongly depends
on the redox state serves to resolve a discrepancy detected during former
studies that obscured the exact position of the AOX in the respiratory chain.
Sulfide oxidation via the alternative pathway was inhibited by
antimycin A; therefore, complex III was thought to be involved in this pathway
without any proton translocation taking place
(Völkel and Grieshaber,
1996; Völkel and
Grieshaber, 1997). In contrast to myxothiazole, antimycin A
stimulates ROS production at complex III, which in turn evidently inhibits the
AOX (Andreyev et al., 2005).
Therefore, the addition of antimycin A can indirectly inhibit sulfide
oxidation via the AOX, although complex III is not involved in the
reaction.
DHA selectively activates the energy-conserving sulfide oxidation pathway
in lugworm mitochondria, probably by preventing the inhibition of cytochrome
oxidase. However, the mechanism of this reaction does not exclusively depend
on the cellular redox state, as GSSG had no activating effect. A non-enzymatic
oxidation of sulfide by DHA can by excluded since hardly any ascorbate was
detectable in the assay. Furthermore, the ratio of oxygen consumed and
thiosulfate produced per molecule of sulfide oxidized was comparable in the
presence and in the absence of DHA
(Hildebrandt and Grieshaber,
2008), whereas less oxygen would be consumed if DHA was used as an
electron acceptor.
H2S has been identified as a signaling molecule in mammals
(Wang, 2002), and the
modification of the susceptibility of cytochrome oxidase towards sulfide by
DHA may be part of a regulatory cascade. Cytochrome oxidase activity is
regulated in a complex manner by NO as well as CO, which favors ROS production
and activates cytoprotective signalling pathways
(Zuckerbraun et al., 2007).
H2S could function in a similar way. Mammalian mitochondria
probably do not contain an alternative oxidase so a mechanism to protect
cytochrome oxidase from sulfide inhibition would be even more advantageous
than in sulfide-adapted invertebrates. As the physiological sulfide
concentrations detected in different tissues are much higher than the
inhibitory concentration for isolated mitochondria
(Wang, 2002), a cytosolic
activating factor is likely to exist in mammals as well.
The present results demonstrate that the mitochondrial sulfide oxidation
pathway in A. marina is suitable for an effective detoxification of
H2S and can be regulated in order to meet different cellular
demands. Nevertheless, additional unknown cytosolic or extracellular sulfide
oxidation enzymes might exist. Furthermore, it is still unknown whether all of
the enzymes involved in mitochondrial sulfide oxidation are localized in the
matrix. The SQR is depicted on the matrix face of the inner mitochondrial
membrane in Fig. 6 because the
optimum at pH 9 indicates a localisation in the alkaline matrix
(Theissen and Martin, 2008).
Thus, H2S has to enter the mitochondria before being oxidized and
also has access to its binding site at cytochrome oxidase. This arrangement
facilitates a regulatory role for H2S. Without further modulators,
half-maximal inhibition of cytochrome oxidase in A. marina is
achieved at 1.5 µmoll–1 H2S
(Völkel and Grieshaber,
1997), which is considerably lower than the Km
value of 9.9 µmoll–1 H2S determined for SQR
(Hildebrandt and Grieshaber,
2008). Therefore, respiration can be completely blocked by
sulfide, and the degree of inhibition could be modified by DHA via a
decrease in H2S affinity of cytochrome oxidase. If the SQR is
oriented towards the intermembrane space, intermediates of sulfide oxidation
have to be transported across the inner mitochondrial membrane so this process
could be regulated as well.
Oxygen affinities of mitochondrial oxidases
Cytochrome oxidase from lugworm mitochondria has a significantly lower
Km value for oxygen than the alternative oxidase. Plant
mitochondria show the same tendency. In different tissues of the soy bean,
Glycine max, Km values between 1.6
µmoll–1 and 9.9 µmoll–1 O2
were determined for the alternative oxidase, as opposed to 0.05–0.15
µmoll–1 for cytochrome oxidase
(Millar et al., 1994;
Millar et al., 1997). Thus,
sulfide detoxification in A. marina is less effective than the
energy-providing pathway via the classical respiratory chain at low
oxygen concentrations. The oxygen affinity of mammalian complex IV is
comparable to the value calculated during energy-conserving sulfide oxidation
in the lugworm mitochondria (Km=0.08–0.8
µmoll–1 O2)
(Gnaiger et al., 1998). The
small but significant difference between the Km values
determined with malate as a substrate and with sulfide in the presence of DHA
may result from conformational changes of cytochrome oxidase in the course of
redox regulation.
Possible role of redox regulation in A. marina in vivo
In marine sediments, high sulfide concentrations often occur in combination
with hypoxia. Due to the lack of an appropriate electron acceptor, the lugworm
mitochondria oxidize sulfide only at low rates during hypoxia and thus it
accumulates in the tissue (Völkel and
Grieshaber, 1994). When the oxygen concentration increases after
an anoxic period, mitochondria produce radicals, which cause much of the
tissue damage known as ischemia-reperfusion injury
(Li and Jackson, 2002). The
elevated sulfide concentration is beneficial during reoxygenation, as
H2S protects the cellular components from oxidative stress
(Geng et al., 2004;
Whiteman et al., 2005).
Furthermore, the more oxidized redox state of the cells activates the
energy-conserving sulfide oxidation pathway and inhibits the AOX. This pathway
is particularly favorable when the oxygen supply is limited, as the available
oxygen can be used for ATP production and for sulfide detoxification
simultaneously.
By contrast, sulfide is rapidly detoxified via the AOX pathway during normoxic periods due to the reducing cellular redox state, and carbon substrates can be used for more effective ATP production.
The present study clearly demonstrates two different pathways of mitochondrial sulfide oxidation in A. marina and conveys a simple method to assay them separately. In contrast to previous assumptions, the partitioning of electron flux between the main respiratory chain and the AOX does not exclusively depend on the sulfide concentration but it is influenced by other physiological factors such as GSH and vitamin C. Since, in the present study, all modulators were applied in physiological concentrations, they are likely to take part in the regulation of sulfide oxidation in vivo, presumably in combination with several other cellular factors, which remain to be identified.
LIST OF ABBREVIATIONS
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Acknowledgments |
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