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Response of Sulfide:Quinone Oxidoreductase to Sulfide Exposure in the Echiuran Worm Urechis Unicinctus

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Response of Sulfide:Quinone Oxidoreductase to Sulfide Exposure in the Echiuran Worm Urechis Unicinctus Mar Biotechnol DOI 10.1007/s10126-011-9408-1 ORIGINAL ARTICLE Response of Sulfide:Quinone Oxidoreductase to Sulfide Exposure in the Echiuran Worm Urechis unicinctus Yu-Bin Ma & Zhi-Feng Zhang & Ming-Yu Shao & Kyoung-Ho Kang & Xiao-Li Shi & Ying-Ping Dong & Jin-Long Li Received: 15 May 2011 /Accepted: 22 September 2011 # Springer Science+Business Media, LLC 2011 Abstract Sulfide is a natural, widely distributed, poisonous U. unicinctus sulfide-induced detoxification mechanism substance, and sulfide:quinone oxidoreductase (SQR) is was also discussed. responsible for the initial oxidation of sulfide in mitochon- dria. In this study, we examined the response of SQR to Keywords Mitochondria . Sulfide detoxification . Sulfide: sulfide exposure (25, 50, and 150 μM) at mRNA, protein, quinone oxidoreductase (SQR) . Urechis unicinctus and enzyme activity levels in the body wall and hindgut of the echiuran worm Urechis unicinctus, a benthic organism living in marine sediments. The results revealed SQR Introduction mRNA expression during sulfide exposure in the body wall and hindgut increased in a time- and concentration- Animals, inhabiting environments such as mudflats, marshes, dependent manner that increased significantly at 12 h and cold seeps, and hydrothermal vents can be periodically or − continuously increased with time. At the protein level, SQR continuously exposed to sulfide (the sum of H2S, HS ,and expression in the two tissues showed a time-dependent S2−) (Julian et al. 2005). Sulfide is a well-known toxin with relationship that increased significantly at 12 h in 50 μM the potential to harm organisms through, for example, sulfide and 6 h in 150 μM, and then continued to increase reversible inhibition of cytochrome c oxidase (Evans 1967; with time while no significant increase appeared after 25 Nicholls 1975), decreased hemoglobin oxygen affinity μM sulfide exposure. SQR enzyme activity in both tissues (Carrico et al. 1978), sulfhemoglobin formation (Bagarinao increased significantly in a time-dependent manner after 50 1992; Kraus et al. 1996), mitochondrial depolarization (Julian μM sulfide exposure. We concluded that SQR expression et al. 2005), coelomocyte death, decreased cell proliferation could be induced by sulfide exposure and that the two (Hance et al. 2008), inhibition of almost 20 enzymes involved tissues studied have dissimilar sulfide metabolic patterns. A in aerobic metabolism (Bagarinao 1992), and oxidative damage to RNA and DNA (Joyner-Matos et al. 2010). Mitochondrial sulfide oxidation is an important mechanism : * : : : Y.-B. Ma Z.-F.: Zhang ( ) M.-Y. Shao X.-L. Shi for reducing sulfide toxicity in sulfide-adapted animals Y.-P. Dong J.-L. Li (Grieshaber and Völkel 1998). Some invertebrates, such as Ministry of Education, Key Laboratory of Marine Genetics the gutless clam Solemya reidi and the lugworm Arenicola and Breeding, Ocean University of China, Qingdao 266003, China marina, use mitochondria to oxidize sulfide and even produce e-mail: [email protected] ATP from the substrate (Powell and Somero 1986; Völkel and Grieshaber 1997). In A. marina mitochondria, electrons from Y.-B. Ma sulfide oxidization are transferred to ubiquinone concurrent Shandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuels, Qingdao Institute of Bioenergy with thiosulfate production (Wohlgemuth et al. 2000). and Bioprocess Technology, Chinese Academy of Sciences, In A. marina, sulfide:quinone oxidoreductase (SQR), Qingdao 266101, China originally molecularly characterized in animal at 2003 (Theissen et al. 2003), is involved in electron transfer from K.-H. Kang Department of Aquaculture, Chonnam National University, sulfide to ubiquinone and converts sulfide to persulfides Yeosu 550749, South Korea (Theissen and Martin 2008). Subsequently, a putative sulfur Mar Biotechnol dioxygenase oxidizes a persulfide molecule into sulfite August 2008 in Yantai (China), were maintained for 1 week and a second persulfide is added to sulfite by a sulfur in an aerated re-circulating seawater aquarium (20±1°C, transferase-rhodanese, producing thiosulfate (Hildebrandt pH 8.25±0.02, and 25‰ salinity), and were fed microalgae and Grieshaber 2008a). Also, in this species, the cellular (Chlorella vulgaris and Mtzschia closterium). Feeding was redox state has been shown to regulate mitochondrial sulfide suspended 24 h prior to experimentation. oxidation (Hildebrandt and Grieshaber 2008b). Recently, the Three sulfide concentrations were used in this study, mitochondrial sulfide oxidation pathway, which involves 25 μM, which was regarded as that of lightly polluted SQR, sulfur dioxygenase (ethylmalonic encephalopathy 1) sediments; 50 μM, equivalent to moderately polluted sedi- and rhodanese, has been validated in mammals (Tiranti et al. ments; and 150 μM, similar to heavily polluted sediments 2009). Figure 1 illustrates the mitochondrial sulfide oxida- (data from our field measurements in Yantai, China). The tion pathway, electron transport, and ATP production in this experiment was conducted in airproof glass tanks. Worms pathway. However, whether these sulfide metabolic enzymes were randomly assigned to four groups, three sulfide treat- function under an in vivo sulfide environment is not known. ments and a control (natural seawater). Five worms were In addition, information on their expression regulation after placed in a 10 L water tank containing 7.5 L of seawater and a sulfide exposure is also lacking. Investigations which could total of 28 tanks were used in the experiment. The sulfide help explain sulfide metabolic adaptation in sulfide-adapted concentrations in treatment groups were produced by sodium animals have not been reported. sulfide (Na2S–9H2O), and maintained by sodium sulfide Echiurans are often found in habitats with high sulfide compensation at 2 h intervals. The sulfide level was levels. For example, Urechis caupo (Echiura) is a sulfide- monitored using a spectrophotometer and the methylene adapted animal found along the coast of California and is blue method (Cline 1969). Three worms were removed from close to the well-studied A. marina in ecology habitat and tanks at 0, 0.5, 2, 6, 12, 24, and 48 h after initiation of sulfide phylogenetic tree. Studies on this species have included exposure. The body wall and hindgut of the worms were morphological adaptations of tissues to sulfide, including excised, frozen in liquid nitrogen, and stored at −80°C for unusual organelles named sulfide-oxidizing bodies (Menon subsequently analysis. and Arp 1992;MenonandArp1993;MenonandArp1998), aerobic respiration (Eaton and Arp 1993), hydrogen sulfide Quantitative Analysis of SQR mRNA Expression in Tissues oxidation of heme compounds (Powell and Arp 1989;Arpet al. 1995, review), and sulfide oxidation product (Bogan et al. Total RNA was extracted from the body wall and hindgut 1992;BoganandArp1993) and its elimination (Julian et al. with Trizol (Invitrogen) according to the manufacturer’s 1999). Urechis unicinctus, a species related to U. caupo,is protocol. RNA quality was assessed by 1% agarose gel mainly distributed in China, Korea, Russia, and Japan and electrophoresis, and the RNA concentration and purity inhabits marine sediments, especially in intertidal and determined from the absorbances at 260 and 280 nm. First- subtidal mudflats (Li et al. 1994). This species has sulfide strand cDNA was synthesized using a reverse transcription metabolic adaptations similar to those of U. caupo (Zhang et system (Promega). The cDNA mixture was diluted (1:5) to al. 2003; 2006; Ma et al. 2005; Wang et al. 2010). a final concentration of approximately 240 ng/μl, and then Furthermore, we demonstrated that U. unicinctus could stored at −20°C for later real-time PCR. produce ATP from sulfide as the only substrate, which is Real-time PCR was performed using a fluorescence similar to A. marina (Ma et al. 2010), and recombinant U. temperature cycler (PE Applied Biosystems, 7500 Real- unicinctus SQR expression in Escherichia coli could catalyze Time PCR Systems) and SYBR Green I as a double- sulfide oxidation in vitro (Km for sulfide 40.3 μM) (Ma et al. stranded DNA-specific binding dye. The optimized reactions 2011). In this study, to extend the understanding of sulfide of the real-time PCR were conducted according to manufac- metabolic adaptations, we present the SQR dynamic change turer’s instructions (Toyobo) using β-actin as the internal during mRNA expression, protein expression, and enzyme standard. The primer sequences were: 5′-CTGGCAG activity in the body wall and hindgut of U. unicinctus when CATGTCAAGAAAA-3′ (sense) and 5′-GAGCTCCAGCA exposed to sulfide in the laboratory. CATTTGACA-3′ (antisense) for SQR; and 5′- TTCTTGGGAATGGAATCTGC-3′ (sense) and 5′- CTTCTGCATACGGTCAGCAA-3′ (antisense) for β-actin. Materials and Methods Amplifications were carried out using 10 μL of 2× SYBR Green PCR Master Mix, 1 μLofeachprimer(2μM), 1 μL Animals and Exposure to Sulfide of cDNA in a total volume of 20 μL. Real-time PCR conditions were 95°C for 10 min, followed by 40 cycles at Individuals of U. unicinctus (mean fresh mass of 33.4± 95°C for 15 s, and 60°C for 1 min. Full-length sequences of 10.4 g), collected from a coastal intertidal flat during SQR (GenBank accession number: EF487538) and β-actin Mar Biotechnol Fig. 1 Model of the mitochondrial sulfide oxidation pathway, electron transport, and ATP production during sulfide oxidation (modified from + + 4H 2H Grieshaber and Völkel 1998; Intermembrane space Cyt c Kabil and Banerjee 2010; Hildebrandt
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