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Sulfur Metabolism in Phototrophic Bacteria

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Modern Topics in the Phototrophic Prokaryotes

Abstract

Sulfur is one of the most versatile elements in life due to its reactivity in different oxidation and reduction states. In contrast to the assimilatory provision of sulfur-containing cell constituents that is found in most taxonomic groups, dissimilation is restricted to prokaryotes and serves energy-yielding processes where sulfur compounds are donors or acceptors of electrons. In many anoxygenic phototrophic bacteria, reduced sulfur compounds play a prominent role as electron donors for photosynthetic carbon dioxide fixation. This process is especially characteristic for the green sulfur bacteria (GSB) and the purple sulfur bacteria (PSB). Allochromatium vinosum and Chlorobaculum tepidum , representatives of the PSB and GSB, respectively, are the workhorses for detailed elucidation of sulfur oxidation pathways. Genes identified in these organisms served as the basis of a genome-based survey of the distribution of genes involved in the oxidation of sulfur compounds in other genome-sequenced anoxygenic phototrophs. These analyses show that dissimilatory sulfur metabolism is very complex and built together from various modules encoding different enzymes in the different organisms. Comparative genomics in combination with biochemical data also provide a clear picture of sulfate assimilation in anoxygenic phototrophs.

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References

  • Appia-Ayme C, Little PJ, Matsumoto Y et al (2001) Cytochrome complex essential for photosynthetic oxidation of both thiosulfate and sulfide in Rhodovulum sulfidophilum. J Bacteriol 183:6107–6118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arieli B, Padan E, Shahak Y (1991) Sulfide-induced sulfide—quinone reductase acitivity in thylakoids of Oscillatoria limnetica. J Biol Chem 266:104–111

    CAS  PubMed  Google Scholar 

  • Arieli B, Shahak Y, Taglicht D et al (1994) Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J Biol Chem 269:5705–5711

    CAS  PubMed  Google Scholar 

  • Auernik KS, Kelly RM (2010) Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by transcriptomic analysis of heterotrophic, autotrophic, and mixotrophic growth. Appl Environ Microbiol 76:931–935

    Article  CAS  PubMed  Google Scholar 

  • Baldock MI, Denger K, Smits THM et al (2007) Roseovarius sp. strain 217: aerobic taurine dissimilation via acetate kinase and acetate-CoA ligase. FEMS Microbiol Lett 271:202–206

    Article  CAS  PubMed  Google Scholar 

  • Bamford VA, Bruno S, Rasmussen T et al (2002) Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme. EMBO J 21:5599–5610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbosa-Jefferson VL, Zhao FJ, Mcgrath SP et al (1998) Thiosulphate and tetrathionate oxidation in arable soils. Soil Biol Biochem 30:553–559

    Article  CAS  Google Scholar 

  • Bartsch RG (1978) Cytochromes. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 249–279

    Google Scholar 

  • Bobadilla Fazzini RA, Cortes MP, Padilla L et al (2013) Stoichiometric modeling of oxidation of reduced inorganic sulfur compounds (Riscs) in Acidithiobacillus thiooxidans. Biotechnol Bioeng 110:2242–2251

    Article  CAS  PubMed  Google Scholar 

  • Bosshard HR, Davidson MW, Knaff DB et al (1986) Complex formation and electron transfer between mitochondrial cytochrome c and flavocytochrome c552 from Chromatium vinosum. J Biol Chem 261:190–193

    CAS  PubMed  Google Scholar 

  • Boughanemi S, Lyonnet J, Infossi P et al (2016) Microbial oxidative sulfur metabolism: biochemical evidence of the membrane-bound heterodisulfide reductase-like complex of the bacterium Aquifex aeolicus. FEMS Microbiol Lett 363

    Google Scholar 

  • Bradley JM, Marritt SJ, Kihlken MA et al (2012) Redox and chemical activities of the hemes in the sulfur oxidation pathway enzyme SoxAX. J Biol Chem 287:40350–40359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brito JA, Denkmann K, Pereira IAC et al (2015) Thiosulfate dehydrogenase (TsdA) from Allochromatium vinosum: Structural and functional insights into thiosulfate oxidation. J Biol Chem 290:9222–9238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brito JA, Sousa FL, Stelter M et al (2009) Structural and functional insights into sulfide:quinone oxidoreductase. Biochemistry 48:5613–5622

    Article  CAS  PubMed  Google Scholar 

  • Bronstein M, Schütz M, Hauska G et al (2000) Cyanobacterial sulfide-quinone reductase: cloning and heterologous expression. J Bacteriol 182:3336–3344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brune DC (1989) Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975:189–221

    Article  CAS  PubMed  Google Scholar 

  • Brune DC (1995a) Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersicina. Arch Microbiol 163:391–399

    Article  CAS  PubMed  Google Scholar 

  • Brune DC (1995b) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 847–870

    Google Scholar 

  • Bryant DA, Costas AMG, Maresca JA et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317:523–526

    Article  CAS  PubMed  Google Scholar 

  • Bryantseva IA, Gorlenko VM, Kompantseva EI et al (1999) Thiorhodospira sibirica gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium from a Siberian Soda lake. Int J Syst Bacteriol 49:697–703

    Article  PubMed  Google Scholar 

  • Caumette P, Guyoneaud R, Imhoff JF et al (2004) Thiocapsa marina sp. nov., a novel, okenone-containing, purple sulfur bacterium isolated from brackish coastal and marine environments. Int J Syst Evol Microbiol 54:1031–1036

    Article  CAS  PubMed  Google Scholar 

  • Challacombe JF, Majid S, Deole R et al (2013) Complete genome sequence of Halorhodospira halophila SL1. Stand Genomic Sci 8:206–214

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chan L-K, Morgan-Kiss R, Hanson TE (2009) Functional analysis of three sulfide:quinone oxidoreductase homologs in Chlorobaculum tepidum. J Bacteriol 191:1026–1034

    Article  CAS  PubMed  Google Scholar 

  • Chen ZW, Koh M, van Driessche G et al (1994) The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266:430–432

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Ren Y, Lin J et al (2012) Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One 7:e39470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cherney MM, Zhang Y, Solomonson M et al (2010) Crystal structure of sulfide:quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 398:292–305

    Article  CAS  PubMed  Google Scholar 

  • Christensen QH, Cronan JE (2010) Lipoic acid synthesis: a new family of octanoyltransferases generally annotated as lipoate protein ligases. Biochemistry 49:10024–10036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen QH, Martin N, Mansilla MC et al (2011) A novel amidotransferase required for lipoic acid cofactor assembly in Bacillus subtilis. Mol Microbiol 80:350–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C et al (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    Article  CAS  PubMed  Google Scholar 

  • Cort JR, Selan UM, Schulte A et al (2008) Allochromatium vinosum DsrC: solution-state NMR structure, redox properties and interaction with DsrEFH, a protein essential for purple sulfur bacterial sulfur oxidation. J Mol Biol 382:692–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cusanovich MA, Bartsch RG (1969) A high potential cytochrome c from Chromatium vinosum chromatophores. Biochim Biophys Acta 189:245–255

    Article  CAS  PubMed  Google Scholar 

  • D’Errico G, Di Salle A, La Cara F et al (2006) Identification and characterization of a novel bacterial sulfite oxidase with no heme binding domain from Deinococcus radiodurans. J Bacteriol 188:694–701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dahl C (1996) Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology 142:3363–3372

    Article  CAS  PubMed  Google Scholar 

  • Dahl C (2008) Inorganic sulfur compounds as electron donors in purple sulfur bacteria. In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Sulfur in phototrophic organisms. Springer, Dordrecht, pp 289–317

    Chapter  Google Scholar 

  • Dahl C (2015) Cytoplasmic sulfur trafficking in sulfur-oxidizing prokaryotes. Iubmb Life 67:268–274

    Article  CAS  PubMed  Google Scholar 

  • Dahl C, Friedrich CG, Kletzin A (2008a) Sulfur oxidation in prokaryotes. In: Encyclopedia of Life Sciences (ELS), John Wiley & Sons, Ltd., Chichester, p http://www.els.net/ [DOI: 10.1002/9780470015902.a0021155]

  • Dahl C, Hell R, Leustek T, Knaff DB (2008b) Introduction to sulfur metabolism in phototrophic organisms. In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, pp 1–14

    Chapter  Google Scholar 

  • Dahl C, Schulte A, Stockdreher Y et al (2008c) Structural and molecular genetic insight into a wide-spread bacterial sulfur oxidation pathway. J Mol Biol 384:1287–1300

    Article  CAS  PubMed  Google Scholar 

  • Dahl C, Engels S, Pott-Sperling AS et al (2005) Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol 187:1392–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahl C, Franz B, Hensen D et al (2013) Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process. Microbiology 159:2626–2638

    Article  CAS  PubMed  Google Scholar 

  • Demmer JK, Huang H, Wang S et al (2015) Insights into flavin-based electron bifurcation via the NADH-dependent reduced ferredoxin:NADP oxidoreductase structure. J Biol Chem 290:21985–21995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denger K, Smits THM, Cook AM (2006) Genome-enabled analysis of the utilization of taurine as sole source of carbon or of nitrogen by Rhodobacter sphaeroides 2.4.1. Microbiology 152:3197–3206

    Article  CAS  PubMed  Google Scholar 

  • Denger K, Weinitschke S, Hollemeyer K et al (2004) Sulfoacetate generated by Rhodopseudomonas palustris from taurine. Arch Microbiol 182:154–158

    Article  CAS  Google Scholar 

  • Denkmann K, Grein F, Zigann R et al (2012) Thiosulfate dehydrogenase: a wide-spread unusual acidophilic c-type cytochrome. Environ Microbiol 14:2673–2688

    Article  CAS  PubMed  Google Scholar 

  • Dhillon A, Goswami S, Riley M et al (2005) Domain evolution and functional diversification of sulfite reductases. Astrobiology 5:18–29

    Article  CAS  PubMed  Google Scholar 

  • Eddie BJ, Hanson TE (2013) Chlorobaculum tepidum TLS displays a complex transcriptional response to sulfide addition. J Bacteriol 195:399–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrenfeld N, Levicán G, Parada P (2013) Heterodisulfide reductase from Acdidithiobacilli is a key component involved in metabolism of reduced inorganic sulfur compounds. Adv Mater Res 825:194–197

    Article  CAS  Google Scholar 

  • Falkenby LG, Szymanska M, Holkenbrink C et al (2011) Quantitative proteomics of Chlorobaculum tepidum: insights into the sulfur metabolism of a phototrophic green sulfur bacterium. FEMS Microbiol Lett 323:142–150

    Article  CAS  PubMed  Google Scholar 

  • Foster BA, Thomas SM, Mahr JA et al (1994) Cloning and sequencing of ATP sulfurylase from Penicillium chrysogenum: identification of a likely allosteric domain. J Biol Chem 269:19777–19786

    CAS  PubMed  Google Scholar 

  • Franz B, Gehrke T, Lichtenberg H et al (2009) Unexpected extracellular and intracellular sulfur species during growth of Allochromatium vinosum with reduced sulfur compounds. Microbiology 155:2766–2774

    Article  CAS  PubMed  Google Scholar 

  • Franz B, Lichtenberg H, Hormes J et al (2007) Utilization of solid “elemental” sulfur by the phototrophic purple sulfur bacterium Allochromatium vinosum: a sulfur K-edge XANES spectroscopy study. Microbiology 153:1268–1274

    Article  CAS  PubMed  Google Scholar 

  • Friedrich CG, Bardischewsky F, Rother D et al (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259

    Article  CAS  PubMed  Google Scholar 

  • Friedrich CG, Rother D, Bardischewsky F et al (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frigaard N-U, Bryant DA (2008a) Genomic and evolutionary perspectives on sulfur metabolism in green sulfur bacteria. In: Dahl C, Friedrich CG (eds) Microbial sulfur metabolism. Springer, Heidelberg, Heidelberg, pp 60–76

    Chapter  Google Scholar 

  • Frigaard N-U, Bryant DA (2008b) Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, pp 337–355

    Chapter  Google Scholar 

  • Frigaard N-U, Dahl C (2009) Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54:103–200

    Article  CAS  PubMed  Google Scholar 

  • Funane K, Iwahashi H, Nakamura T (1987) Metabolism of S-sulfocysteine in Salmonella typhimurium. Role of thioredoxin in the reduction of S-sulfocysteine. Agric Biol Chem 51:1247–1256

    CAS  Google Scholar 

  • Gregersen LH, Bryant DA, Frigaard N-U (2011) Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front Microbiol 2:116. doi:10.3389/fmicb.2011.00116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grein F, Pereira IAC, Dahl C (2010a) The Allochromatium vinsosum DsrMKJOP transmembrane complex: biochemical characterization of individual components aids understanding of complex function in vivo. J Bacteriol 192:6369–6377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grein F, Ramos AR, Venceslau SS et al (2013) Unifying concepts in anaerobic respiration: Insights from dissimilatory sulfur metabolism. Biochim Biophys Acta 1827:145–160

    Article  CAS  PubMed  Google Scholar 

  • Grein F, Venceslau SS, Schneider L et al (2010b) DsrJ, an essential part of the DsrMKJOP complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c. Biochemistry 49:8290–8299

    Article  CAS  PubMed  Google Scholar 

  • Griesbeck C, Schütz M, Schödl T et al (2002) Mechanism of sulfide-quinone oxidoreductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Yin H, Liang Y et al (2014) Comparative genome analysis reveals metabolic versatility and environmental adaptations of Sulfobacillus thermosulfidooxidans strain ST. PLoS One 9:e99417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hamilton TL, Bovee RJ, Thiel V et al (2014) Coupled reductive and oxidative sulfur cycling in the phototrophic plate of a meromictic lake. Geobiology 12:451–468

    Article  CAS  PubMed  Google Scholar 

  • Hedderich R, Hamann N, Bennati M (2005) Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster. Biol Chem 386:961–970

    Article  CAS  PubMed  Google Scholar 

  • Heinzinger NK, Fujimoto SY, Clark MA et al (1995) Sequence analysis of the phs operon in Salmonella typhimurium and the contribution of thiosulfate reduction to anaerobic energy metabolism. J Bacteriol 177:2813–2820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hensel G, Trüper HG (1976) Cysteine and S-sulfocysteine biosynthesis in phototrophic bacteria. Arch Microbiol 109:101–103

    Article  CAS  PubMed  Google Scholar 

  • Hensel M, Hinsley AP, Nikolaus T et al (1999) The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol 32:275–287

    Article  CAS  PubMed  Google Scholar 

  • Hensen D, Sperling D, Trüper HG et al (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62:794–810

    Article  CAS  PubMed  Google Scholar 

  • Hipp WM, Pott AS, Thum-Schmitz N et al (1997) Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143:2891–2902

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF (2001) Transfer of Pfennigia purpurea Tindall 1999 (Amoebobacter purpureus Eichler and Pfennig 1988) to the genus Lamprocystis as Lamprocystis purpurea comb. nov. Int J Syst Evol Microbiol 51:1699–1701

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF (2003) Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna-Matthews-Olson protein) gene sequences. Int J Syst Evol Microbiol 53:941–951

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF, Pfennig N (2001) Thioflavicoccus mobilis gen. nov., sp nov., a novel purple sulfur bacterium with bacteriochlorophyll b. Int J Syst Evol Microbiol 51:105–110

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF, Süling J (1996) The phylogenetic relationship among Ectothiorhodospiraceae: a reevalution of their taxonomy on the basis of 16S rDNA analyses. Arch Microbiol 165:106–113

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF, Hiraishi A, Süling J (2005) Anoxygenic phototrophic purple bacteria. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 119–132

    Chapter  Google Scholar 

  • Imhoff JF, Süling J, Petri R (1998) Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa, and Thermochromatium. Int J Syst Bacteriol 48:1129–1143

    Article  PubMed  Google Scholar 

  • Jormakka M, Yokoyama K, Yano T et al (2008) Molecular mechanism of energy conservation in polysulfide respiration. Nat Struct Mol Biol 15:730–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kappler U, Bailey S (2005) Molecular basis of intramolecular electron transfer in sulfite-oxidizing enzymes is revealed by high resolution structure of a heterodimeric complex of the catalytic molybdopterin subunit and a c-type cytochrome subunit. J Biol Chem 280:24999–25007

    Article  CAS  PubMed  Google Scholar 

  • Kappler U, Schäfer H (2014) Transformations of dimethylsulfide. Met Ions Life Sci 14:279–313

    Article  PubMed  Google Scholar 

  • Kappler U, Bennett B, Rethmeier J et al (2000) Sulfite: cytochrome c oxidoreductase from Thiobacillus novellus—Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J Biol Chem 275:13202–13212

    Article  CAS  PubMed  Google Scholar 

  • Kappler U, Bernhardt PV, Kilmartin J et al (2008) SoxAX cytochromes, a new type of heme copper protein involved in bacterial energy generation from sulfur compounds. J Biol Chem 283:22206–22214

    Article  CAS  PubMed  Google Scholar 

  • Khanna S, Nicholas DJD (1982) Utilization of tetrathionate and 35S-labelled thiosulphate by washed cells of Chlorobium vibrioforme f. sp. thiosulfatophilum. J Gen Microbiol 128:1027–1034

    CAS  Google Scholar 

  • Koblizek M (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev 39:854–870

    Article  PubMed  Google Scholar 

  • Kostanjevecki V, Brige A, Meyer TE et al (2000) A membrane-bound flavocytochrome c-sulfide dehydrogenase from the purple phototrophic sulfur bacterium Ectothiorhodospira vacuolata. J Bacteriol 182:3097–3103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krafft T, Bokranz M, Klimmek O et al (1992) Cloning and nucleotide sequence of the psrA gene of Wolinella succinogenes polysulphide reductase. Eur J Biochem 206:503–510

    Article  CAS  PubMed  Google Scholar 

  • Kredich NM (1992) The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli. Mol Microbiol 6:2747–2753

    Article  CAS  PubMed  Google Scholar 

  • Kredich NM (1996) Biosynthesis of cysteine. In: Neidhardt FC (ed) Escherichia coli and Salmonella typhimurium. Cellular and molecular biology. American Society for Microbiology, Washington, pp 514–527

    Google Scholar 

  • Kulp TR, Hoeft SE, Asao M et al (2008) Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from mono lake, California. Science 321:967–970

    Article  CAS  PubMed  Google Scholar 

  • Kurth J, Dahl C, Butt JN (2015) Catalytic protein film electrochemistry provides a direct measure of the tetrathionate/thiosulfate reduction potential. J Am Chem Soc 137:13232–13235

    Article  CAS  PubMed  Google Scholar 

  • Laska S, Lottspeich F, Kletzin A (2003) Membrane-bound hydrogenase and sulfur reductase of the hyperthermophilic and acidophilic archaeon Acidianus ambivalens. Microbiology 149:2357–2371

    Article  CAS  PubMed  Google Scholar 

  • Latorre M, Ehrenfeld N, Cortes MP et al (2016) Global transcriptional responses of Acidithiobacillus ferrooxidans Wenelen under different sulfide minerals. Bioresour Technol 200:29–34

    Article  CAS  PubMed  Google Scholar 

  • Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leyh TS (1993) The physical biochemistry and molecular genetics of sulfate activation. Crit Rev Biochem Mol Biol 28:515–542

    Article  CAS  PubMed  Google Scholar 

  • Liu Y-W, Denkmann K, Kosciow K et al (2013) Tetrathionate stimulated growth of Campylobacter jejuni identifies TsdA as a new type of bi-functional tetrathionate reductase that is widely distributed in bacteria. Mol Microbiol 88:188

    Article  CAS  Google Scholar 

  • Lu W-P, Kelly DP (1988) Respiration-driven proton translocation in Thiobacillus versutus and the role of the periplasmic thiosulphate-oxidizing enzyme system. Arch Microbiol 149:297–302

    Article  CAS  Google Scholar 

  • Lübbe YJ, Youn H-S, Timkovich R et al (2006) Siro(haem)amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a,c diamide synthase for sulphur oxidation. FEMS Microbiol Lett 261:194–202

    Article  PubMed  CAS  Google Scholar 

  • MacRae IJ, Segel IH, Fisher AJ (2001) Crystal structure of ATP sulfurylase from Penicillium chrysogenum: insights into the allosteric regulation of sulfate assimilation. Biochemistry 40:6795–6804

    Article  CAS  PubMed  Google Scholar 

  • Mangold S, Valdés J, Holmes DS et al (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front Microbiol. doi:10.3389/fmcib.2011.00017

    PubMed  PubMed Central  Google Scholar 

  • Marcia M, Ermler U, Peng GH et al (2010a) A new structure-based classification of sulfide:quinone oxidoreductases. Proteins: Struct, Funct, Bioinf 78:1073–1083

    Article  CAS  Google Scholar 

  • Marcia M, Langer JD, Parcej D et al (2010b) Characterizing a monotopic membrane enzyme. Biochemical, enzymatic and crystallization studies on Aquifex aeolicus sulfide:quinone oxidoreductase. Biochim Biophys Acta, Biomembr 1798:2114–2123

    Article  CAS  Google Scholar 

  • Marcia M, Ermler U, Peng GH et al (2009) The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc Natl Acad Sci U S A 106:9625–9630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marnocha CL, Levy AT, Powell DH et al (2016) Mechanisms of extracellular S(0) globule production and degradation in Chlorobaculum tepidum via dynamic cell-globule interactions. Microbiology 162(7):1125–1134

    Article  CAS  PubMed  Google Scholar 

  • Meyer TE, Cusanovich MA (2003) Discovery and characterization of electron transfer proteins in the photosynthetic bacteria. Photosynth Res 76:111–126

    Article  CAS  PubMed  Google Scholar 

  • Meyer B, Kuever J (2007) Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153:3478–3498

    Article  CAS  PubMed  Google Scholar 

  • Meyer B, Imhoff JF, Kuever J (2007) Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria—evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 9:2957–2977

    Article  CAS  PubMed  Google Scholar 

  • Middelburg J (2000) The geochemical sulfur cycle. In: Lens P, Hulshoff Pol W (eds) Environmental technologies to treat sulfur pollution. IWA Publishing, London, pp 33–46

    Google Scholar 

  • Müller FH, Bandeiras TM, Urich T et al (2004) Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate:quinone oxidoreductase. Mol Microbiol 53:1147–1160

    Article  PubMed  CAS  Google Scholar 

  • Nakatani T, Ohtsu I, Nonaka G et al (2012) Enhancement of thioredoxin/glutaredoxin-mediated L-cysteine synthesis from S-sulfocysteine increases L-cysteine production in Escherichia coli. Microb Cell Fact 11:62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann S, Wynen A, Trüper HG et al (2000) Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway. Mol Biol Rep 27:27–33

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T, Furusawa T, Nomura R et al (2008) SoxAX binding protein, a novel component of the thiosulfate-oxidizing multienzyme system in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 190:6097–6110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osorio H, Mangold S, Denis Y et al (2013) Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 79:2172–2181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang J, Liu Q, Li B et al (2013) Proteomic analysis of differential protein expression in Acidithiobacillus ferrooxidans grown on ferrous iron or elemental sulfur. Indian J Microbiol 53:56–62

    Article  CAS  PubMed  Google Scholar 

  • Parey K, Demmer U, Warkentin E et al (2013) Structural, biochemical and genetic characterization of ATP sulfurylase from Allochromatium vinosum. PLoS One 8:e74707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattaragulwanit K, Brune DC, Trüper HG et al (1998) Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum. Arch Microbiol 169:434–444

    Article  CAS  PubMed  Google Scholar 

  • Pires RH, Lourenco AI, Morais F et al (2003) A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta 1605:67–82

    Article  CAS  PubMed  Google Scholar 

  • Pires RH, Venceslau SS, Morais F et al (2006) Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex—a membrane-bound redox complex involved in the sulfate respiratory pathway. Biochemistry 45:249–262

    Article  CAS  PubMed  Google Scholar 

  • Podgorsek L, Imhoff JF (1999) Tetrathionate production by sulfur oxidizing bacteria and the role of tetrathionate in the sulfur cycle of Baltic Sea sediments. Aquat Microb Ecol 17:255–265

    Article  Google Scholar 

  • Pott AS, Dahl C (1998) Sirohaem-sulfite reductase and other proteins encoded in the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881–1894

    Article  CAS  PubMed  Google Scholar 

  • Prange A, Chauvistré R, Modrow H et al (2002) Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different speciations of sulfur. Microbiology 148:267–276

    Article  CAS  PubMed  Google Scholar 

  • Prange A, Engelhardt H, Trüper HG et al (2004) The role of the sulfur globule proteins of Allochromatium vinosum: mutagenesis of the sulfur globule protein genes and expression studies by real-time RT PCR. Arch Microbiol 182:165–174

    Article  CAS  PubMed  Google Scholar 

  • Quatrini R, Appia-Ayme C, Denis Y et al (2006) Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263–272

    Article  CAS  Google Scholar 

  • Quatrini R, Appia-Ayme C, Denis Y et al (2009) Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics 10:394

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quentmeier A, Friedrich CG (2001) The cysteine residue of the SoxY protein as the active site of protein-bound sulfur oxidation of Paracoccus pantotrophus GB17. FEBS Lett 503:168–172

    Article  CAS  PubMed  Google Scholar 

  • Ramos AR, Keller KL, Wall JD et al (2012) The membrane QmoABC complex interacts directly with the dissimilatory adenosine 5′-phosphosulfate reductase in sulfate reducing bacteria. Front Microbiol 3:137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond JC, Sistrom WR (1969) Ectothiorhodospira halophila—a new species of the genus Ectothiorhodospira. Arch Mikrobiol 69:121–126

    Article  CAS  PubMed  Google Scholar 

  • Reijerse EJ, Sommerhalter M, Hellwig P et al (2007) The unusal redox centers of SoxXA, a novel c-type heme-enzyme essential for chemotrophic sulfur-oxidation of Paracoccus pantotrophus. Biochemistry 46:7804–7810

    Article  CAS  PubMed  Google Scholar 

  • Reinartz M, Tschäpe J, Brüser T et al (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170:59–68

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez J, Hiras J, Hanson TE (2011) Sulfite oxidation in Chlorobaculum tepidum. Front Microbiol 2:112. doi:10.3389/fmcib.2011.00112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez O, Ferrera I, Dahl C et al (2001) In vivo role of APS reductase in the purple sulfur bacterium Allochromatium vinosum. Arch Microbiol 176:301–305

    Article  CAS  PubMed  Google Scholar 

  • Sander J, Dahl C (2009) Metabolism of inorganic sulfur compounds in purple bacteria. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) Purple bacteria. Springer, Dordrecht, pp 595–622

    Chapter  Google Scholar 

  • Sander J, Engels-Schwarzlose S, Dahl C (2006) Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch Microbiol 186:357–366

    Article  CAS  PubMed  Google Scholar 

  • Santos AA, Venceslau SS, Grein F et al (2015) A protein trisulfide couples dissimilatory sulfate reduction to energy conservation. Science 350:1541–1545

    Article  CAS  PubMed  Google Scholar 

  • Sauvé V, Bruno S, Berks BC et al (2007) The SoxYZ complex carries sulfur cycle intermediates on a peptide swinging arm. J Biol Chem 282:23194–23204

    Article  PubMed  CAS  Google Scholar 

  • Sauvé V, Roversi P, Leath KJ et al (2009) Mechanism for the hydrolysis of a sulfur-sulfur bond based on the crystal structure of the thiosulfohydrolase SoxB. J Biol Chem 284:21707–21718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schütz M, Maldener I, Griesbeck C et al (1999) Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J Bacteriol 181:6516–6523

    PubMed  PubMed Central  Google Scholar 

  • Schütz M, Shahak Y, Padan E et al (1997) Sulfide-quinone reductase from Rhodobacter capsulatus. J Biol Chem 272:9890–9894

    Article  PubMed  Google Scholar 

  • Sekowska A, Kung HF, Danchin A (2000) Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2:145–177

    CAS  PubMed  Google Scholar 

  • Shahak Y, Hauska G (2008) Sulfide oxidation from cyanobacteria to humans: sulfide-quinone oxidoreductase (SQR). In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, pp 319–335

    Chapter  Google Scholar 

  • Shuman KE, Hanson TE (2016) A sulfide:quinone oxidoreductase from Chlorobaculum tepidum displays unusual kinetic properties. FEMS Microbiol Lett 363

    Google Scholar 

  • Simon J, Kern M (2008) Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial respiration. Biochem Soc Trans 36:1011–1016

    Article  CAS  PubMed  Google Scholar 

  • Simon J, Kroneck PM (2013) Microbial sulfite respiration. Adv Microb Physiol 62:45–117

    Article  CAS  PubMed  Google Scholar 

  • Singh KS, Kirksey J, Hoff WD et al (2014) Draft genome sequence of the extremely halophilic phototrophic purple sulfur bacterium Halorhodospira halochloris. J Genet 2:118–120

    Google Scholar 

  • Sirko A, Zatyka M, Sadowy E et al (1995) Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins. J Bacteriol 177:4134–4136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith AJ, Lascelles J (1966) Thiosulphate metabolism and rhodanese in Chromatium sp. strain D. J Gen Microbiol 42:357–370

    Article  CAS  PubMed  Google Scholar 

  • Sorokin DY (2003) Oxidation of inorganic sulfur compounds by obligately organotrophic bacteria. Microbiology 72:641–653

    Article  CAS  Google Scholar 

  • Sorokin DY, Tourova TP, Kuznetsov BB et al (2000) Roseinatronobacter thiooxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll a—containing bacterium isolated from a soda lake. Microbiology 69:75–82

    Article  CAS  Google Scholar 

  • Spalding MD, Prigge ST (2010) Lipoic acid metabolism in microbial pathogens. Microbiol Mol Biol Rev 74:200–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spring S (2014) Function and evolution of the Sox multienzyme complex in the marine Gammaproteobacterium Congregibacter litoralis. ISRN Microbiol 2014:597418

    Article  PubMed  PubMed Central  Google Scholar 

  • Steudel R, Holdt G, Visscher PT et al (1990) Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Arch Microbiol 155:432–437

    Article  Google Scholar 

  • Stockdreher Y, Sturm M, Josten M et al (2014) New proteins involved in sulfur trafficking in the cytoplasm of Allochromatium vinosum. J Biol Chem 289:12390–12403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stockdreher Y, Venceslau SS, Josten M et al (2012) Cytoplasmic sulfurtransferases in the purple sulfur bacterium Allochromatium vinosum: evidence for sulfur transfer from DsrEFH to DsrC. PLoS One 7:e40785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tank M, Bryant DA (2015a) Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium. Int J Syst Evol Microbiol 65:1426–1430

    Article  CAS  PubMed  Google Scholar 

  • Tank M, Bryant DA (2015b) Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum. Front Microbiol 6:226

    Article  PubMed  PubMed Central  Google Scholar 

  • Thauer RK, Kaster AK, Seedorf H et al (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591

    Article  CAS  PubMed  Google Scholar 

  • Then J, Trüper HG (1981) The role of thiosulfate in sulfur metabolism of Rhodopseudomonas globiformis. Arch Microbiol 130:143–146

    Article  CAS  Google Scholar 

  • Venceslau SS, Stockdreher Y, Dahl C et al (2014) The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism. Biochim Biophys Acta 1837:1148–1164

    Article  CAS  PubMed  Google Scholar 

  • Visscher PT, Taylor BF (1993) Organic thiols as organolithotrophic substrates for growth of phototrophic bacteria. Appl Environ Microbiol 59:93–96

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weissgerber T, Sylvester M, Kröninger L et al (2014a) A comparative quantitative proteome study identifies new proteins relevant for sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum. Appl Environ Microbiol 80:2279–2292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weissgerber T, Watanabe M, Hoefgen R et al (2014b) Metabolomic profiling of the purple sulfur bacterium Allochromatium vinosum during growth on different reduced sulfur compounds and malate. Metabolomics 10:1094–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weissgerber T, Dobler N, Polen T et al (2013) Genome-wide transcriptional profiling of the purple sulfur bacterium Allochromatium vinosum DSM 180T during growth on different reduced sulfur compounds. J Bacteriol 195:4231–4245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weissgerber T, Zigann R, Bruce D et al (2011) Complete genome sequence of Allochromatium vinosum DSM 180T. Stand Genomic Sci 5:311–330. doi:10.4056/sigs.2335270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welte C, Hafner S, Krätzer C et al (2009) Interaction between Sox proteins of two physiologically distinct bacteria and a new protein involved in thiosulfate oxidation. FEBS Lett 583:1281–1286

    Article  CAS  PubMed  Google Scholar 

  • Wentzien S, Sand W, Albertsen A et al (1994) Thiosulfate and tetrathionate degradation as well as biofilm generation by Thiobacillus intermedius and Thiobacillus versutus studied by microcalorimetry, HPLC, and ion-pair chromatography. Arch Microbiol 161:116–125

    Article  CAS  Google Scholar 

  • Wilson JJ, Kappler U (2009) Sulfite oxidation in Sinorhizobium meliloti. Biochim Biophys Acta 1787:1516–1525

    Article  CAS  PubMed  Google Scholar 

  • Woodin TS, Segel IH (1968) Glutathione reductase-dependent metabolism of cysteine-S-sulfate by Penicillium chrysogenum. Biochim Biophys Acta 167:78–88

    Article  CAS  PubMed  Google Scholar 

  • Yurkov VV, Krasil’nikova EN, Gorlenko VM (1994) Thiosulfate metabolism in the aerobic bacteriochlorophyll-a-containing bacteria Erythromicrobium hydrolyticum and Roseococcus thiosulfatophilus. Microbiology 63:91–94

    Google Scholar 

  • Zaar A, Fuchs G, Golecki JR et al (2003) A new purple sulfur bacterium isolated from a littoral microbial mat, Thiorhodococcus drewsii sp. nov. Arch Microbiol 179:174–183

    Article  CAS  PubMed  Google Scholar 

  • Zander U, Faust A, Klink BU et al (2010) Structural basis for the oxidation of protein-bound sulfur by the sulfur cycle molybdohemo-enzyme sulfane dehydrogenase SoxCD. J Biol Chem 286:8349–8360

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeng Y, Feng F, Medova H et al (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci U S A 111:7795–7800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Y, Selyanin V, Lukes M et al (2015) Characterization of the microaerophilic, bacteriochlorophyll a-containing bacterium Gemmatimonas phototrophica sp. nov., and emended descriptions of the genus Gemmatimonas and Gemmatimonas aurantiaca. Int J Syst Evol Microbiol 65:2410–2419

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Weiner JH (2014) Characterization of the kinetics and electron paramagnetic resonance spectroscopic properties of Acidithiobacillus ferrooxidans sulfide:quinone oxidoreductase (SQR). Arch Biochem Biophys 564:110–119

    Article  CAS  PubMed  Google Scholar 

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Support by the Deutsche Forschungsgenmeinschaft (Grant Da 351/6-2) is gratefully acknowledged.

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Dahl, C. (2017). Sulfur Metabolism in Phototrophic Bacteria. In: Hallenbeck, P. (eds) Modern Topics in the Phototrophic Prokaryotes. Springer, Cham. https://doi.org/10.1007/978-3-319-51365-2_2

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