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Catalytic Properties of Flavocytochrome C Sulfide Dehydrogenase from Haloalkaliphilic Bacterium Thioalkalivibrio Paradoxus

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Catalytic Properties of Flavocytochrome C Sulfide Dehydrogenase from Haloalkaliphilic Bacterium Thioalkalivibrio Paradoxus ISSN 0006-2979, Biochemistry (Moscow), 2021, Vol. 86, No. 3, pp. 361-369. © Pleiades Publishing, Ltd., 2021. Published in Russian in Biokhimiya, 2021, Vol. 86, No. 3, pp. 422-430. Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM20-320, March 8, 2021. Catalytic Properties of Flavocytochrome c Sulfide Dehydrogenase from Haloalkaliphilic Bacterium Thioalkalivibrio paradoxus Tamara V. Tikhonova1,a*, Anastasiya V. Lilina1, Evgenii M. Osipov1, Nikolay S. Shipkov1, Nataliya I. Dergousova1, Olga G. Kulikova1, and Vladimir O. Popov1 1Bach Institute of Biochemistry, Research Centre of Biotechnology, Russian Academy of Sciences, 119071 Moscow, Russia ae-mail: [email protected] Received September 25, 2020 Revised November 23, 2020 Accepted November 23, 2020 Abstract—Flavocytochrome c sulfide dehydrogenase (FCC) is one of the central enzymes of the respiratory chain in sulfur- oxidizing bacteria. FCC catalyzes oxidation of sulfide and polysulfide ions to elemental sulfur accompanied by electron transfer to cytochrome c. The catalytically active form of the enzyme is a non-covalently linked heterodimer composed of flavin- and heme-binding subunits. The Thioalkalivibrio paradoxus ARh1 genome contains five copies of genes encoding homologous FCCs with an amino acid sequence identity from 36 to 54%. When growing on thiocyanate or thiosulfate as the main energy source, the bacterium synthesizes products of different copies of FCC genes. In this work, we isolated and char- acterized FCC synthesized during the growth of Tv. paradoxus on thiocyanate. FCC was shown to oxidize exclusively sulfide but not other reduced sulfur compounds, such as thiosulfate, sulfite, tetrathionate, and sulfur, and it also does not catalyze the reverse reaction of sulfur reduction to sulfide. Kinetic parameters of the sulfide oxidation reaction are characterized. DOI: 10.1134/S0006297921030111 Keywords: sulfur-oxidizing bacteria, flavocytochrome c sulfide dehydrogenase, thiocyanate dehydrogenase, enzyme kinetics INTRODUCTION of sulfur compounds in the energy cycle of the bacteria of the Thioalkalivibrio genus based on the analysis of the Gram-negative sulfur-oxidizing γ-proteobacteria of genomes and transcriptomes of the Thioalkalivibrio bac- the genus Thioalkalivibrio are haloalkaliphilic obligate teria [6]. autotrophs that are found in soda lakes in Africa, Central Flavocytochrome c sulfide dehydrogenase (FCC) is Asia, and North America [1-4]. Microbial communities one of the central enzymes of sulfur metabolism in sulfur- in these lakes have adapted to extreme conditions such as oxidizing bacteria [12-16]. This enzyme catalyzes oxida- extreme alkaline pH levels (up to pH 11) and high salini- tion of sulfide and polysulfide ions to molecular sulfur ty (up to 4 M Na+). Oxidation of the reduced sulfur com- accompanied by electron transfer to cytochrome c. The pounds (thiosulfate, sulfide, polysulfide, and sulfur) catalytically active form of FCC is a non-covalently serves as the main source of energy for the lithoau- linked heterodimer composed of a flavin-binding subunit totrophic microbial communities in soda lakes [1]. Ten (≈45 kDa) and a monoheme c (≈10 kDa) [13, 14] or out of 85 Thioalkalivibrio strains isolated from soda lakes diheme c (≈25 kDa) [12, 15, 16] binding subunit. The are able to grow on thiocyanate (SCN–) as a sole energy flavin-binding subunit of FCC contains a flavin adenine source [2, 5]. Thioalkalivibrio paradoxus ARh 1, Thio- dinucleotide (FAD) molecule covalently bound through a alkalivibrio nitratireducens ALEN 2, and Thioalkalivibrio thioether bond. thiocyanoxidans ARh 2T are the most well-characterized The genome of one of the thiocyanate-oxidizing strains [6-11]. Figure 1 presents main metabolic pathways strains, Thioalkalivibrio paradoxus ARh 1 [6], contains five copies of gene clusters encoding proteins homologous Abbreviations: CytC, cytochrome c from horse heart; FCC, flav- to FCC. The gene of one of the five potential FCCs ocytochrome c sulfide dehydrogenase; TcDH, thiocyanate (hereinafter TpFCC) is located adjacent to the operon dehydrogenase; TpFCC, flavocytochrome c sulfide dehydroge- responsible for biosynthesis of thiocyanate dehydrogenase nase from the bacterium Thioalkalivibrio paradoxus ARh 1. (TcDH), which is a key enzyme of thiocyanate metabo- * To whom correspondence should be addressed. lism in bacteria of the Thioalkalivibrio genus [6, 7, 11]. 361 362 TIKHONOVA et al. Fig. 1. Schematic diagram of oxidation steps of the sulfur cycle in thiocyanate-oxidizing bacteria of the Thioalkalivibrio genus [6]. SQR is sul- fide:quinone oxidoreductase; FCC is flavocytochrome c sulfide dehydrogenase; SoxYZXAB and SoxCD are components of the sulfur-oxidiz- ing system Sox; TcDH is thiocyanate dehydrogenase; DSR is dissimilatory sulfite reductase; SDH is sulfite dehydrogenase; APR is adenosine 5′-phosphosulfate reductase; SAT is sulfate adenylyltransferase. Comparative analysis of the transcriptomes of the bacteri- [FCC and SQR (sulfide:quinone oxidoreductase)], um Thioalkalivibrio thiocyanoxidans ARh 2T grown on including redox-active cysteine residues involved in sul- thiosulfate and thiocyanate as an energy source demon- fide oxidation followed by electron transfer to FAD. strated that expression of the TcDH gene and neighboring Moreover, participation of TpFCC in the oxidation of genes significantly increased when the cells grew on thio- sulfide ions to sulfur has been further confirmed by the cyanate. Maximum increase in the expression levels was presence of an additional sulfur atom as a product of the achieved for the genes encoding TcDH (log2 of the gene reaction at one of the catalytic cysteines [17]. Such struc- expression level ratio during the growth on thiocyanate tures containing chains of two or eight sulfur atoms in the and thiosulfate was 7.5) and FCC (the corresponding log- active site were determined previously for FCC from arithm of the expression level ratio was 6.94 for the flavin Thermochromatium tepidum [16] and SQR from Aquifex subunit of FCC and 5.82 for the heme-containing subunit aeolicus [18, 19]. The electron-transport subunit of of FCC). Other genes in the TcDH cluster show changes TpFCC contains one domain that binds one heme c in the gene expression level in the range from 3.95 to 6.75 coordinated by His and Met residues. The polypeptide [6]. From this it follows that the expression of FCC gene chain fold of the cytochrome subunit is similar to that of in the bacterium Tv. thiocyanoxidans increases specifical- the N-terminal domains of the two-domain cytochrome ly and is strongly associated with the TcDH gene expres- subunits in other FCCs. In the three-dimensional struc- sion level. Presumably, a similar situation occurs with the ture determined in [17], TpFCC exists in complex with closely related bacterium Tv. paradoxus ARh 1. the copper-binding protein CopC, the gene of which is Therefore, TpFCC is a required component of thio- also characterized by the increased level of transcription cyanate metabolism in the bacterium Tv. paradoxus. in the cells growing on thiocyanate. It was suggested [17] However, the role of TpFCC in the thiocyanate metabo- that the TpFCC–CopC complex is a component of a lism is unclear because thiocyanate decomposition larger periplasmic complex, which also includes TcDH. (Fig. 1) does not involve formation of sulfide ions. It was Role of the complex is to oxidize thiocyanate and utilize suggested that TpFCC can be involved in the transfer of the resulting sulfur. electrons generated in the process of thiocyanate oxida- To test these assumptions, in the present study we tion by TcDH [6]. performed functional characterization of TpFCC. It was Previously, TpFCC was isolated as a major protein of shown that, like the FCCs described previously, TpFCC the periplasmic fraction of the bacterium Tv. paradoxus has a narrow substrate specificity and only catalyzes oxi- grown on thiocyanate. The three-dimensional structure dation of sulfide ions. This enzyme does not catalyze oxi- of TpFCC was determined by X-ray crystallography [17]. dation of other anions containing sulfur in the reduced Comparative analysis of the three-dimensional structure state (thiosulfate, tetrathionate, sulfite) as well as oxida- of TpFCC and the structures of FCCs from other organ- tion or reduction of molecular sulfur. Optimal conditions isms confirmed that TpFCC exhibits all characteristic for the in vitro sulfide oxidation were determined. Kinetic features of the active sites of sulfide dehydrogenases parameters of the reaction were evaluated. BIOCHEMISTRY (Moscow) Vol. 86 No. 3 2021 CATALYTIC PROPERTIES OF FLAVOCYTOCHROME c SULFIDE DEHYDROGENASE 363 MATERIALS AND METHODS calculated from the initial parts of kinetic curves of CytC –1 –1 reduction recorded at 550 nm (ε550 = 22500 M cm ). Isolation and purification of TpFCC. Tv. paradoxus Correction for non-enzyme reaction was applied. For this ARh 1 biomass was grown in flasks using a Na2CO3/ purpose, the rate of CytC reduction with sodium sulfide NaHCO3 mineral medium supplemented with 0.6 M was measured in a parallel experiment in the absence of total Na+ at pH 9.75, as described previously [5] in the FCC. All kinetic measurements were performed in tripli- presence of sodium thiocyanate (10 mM) as an energy cate. Sodium sulfide concentration in the solution was and nitrogen source. After all thiocyanate was consumed, determined using Ellman’s reagent [DTNB, dithiobis(2- another portion of thiocyanate was added
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