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Genomic Insights into the Sulfur Metabolism of Phototrophic Green Sulfur Bacteria

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Sulfur Metabolism in Phototrophic Organisms

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 27))

Green sulfur bacteria (GSB) utilize various combinations of sulfide, elemental sulfur, thiosulfate, ferrous iron, and hydrogen for anaerobic photoautotrophic growth. Genome sequence data is currently available for 12 strains of GSB. We present here a genome-based survey of the distribution and phylogenies of genes involved in oxidation of sulfur compounds in these strains. Sulfide:quinone reductase, encoded by sqr, is the only known sulfur-oxidizing enzyme found in all strains. All sulfide-utilizing strains contain the dissimilatory sulfite reductase dsrABCEFHLNMKJOPT genes, which appear to be involved in elemental sulfur utilization. All thiosulfate-utilizing strains have an identical sox gene cluster (soxJXYZAKBW). The soxCD genes found in certain other thiosulfate-utilizing organisms like Paracoccus pantotrophus are absent from GSB. Genes encoding flavocytochrome c (fccAB), adenosine-5'-phosphosulfate reductase (aprAB), ATP-sulfurylase (sat), a homolog of heterodisulfide reductase (qmoABC), and other enzymes related to sulfur utilization are found in some, but not all sulfide-utilizing strains. Other than sqr, Chlorobium ferrooxidans, a Fe2+ -oxidizing organism that cannot grow on sulfide, has no genes obviously involved in oxidation of sulfur compounds. Instead, Chl. ferrooxidans possesses genes involved in assimilatory sulfate reduction (cysIHDNCG), a trait that is not found in most other GSB. Given the irregular distribution of certain enzymes (such as FccAB, AprAB, Sat, QmoABC) among GSB strains, it appears that different enzymes may produce the same sulfur oxidation phenotype in different strains. Finally, even though the GSB are closely related, sequence analyses show that the sulfur metabolism gene content in these bacteria is substantially influenced by gene duplication and elimination and by lateral gene transfer both within the GSB phylum and with prokaryotes from other phyla.

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References

  • Anderson GL, Williams J and Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem 267:23674–23682

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ashida H, Saito Y, Kojima C, Kobayashi K, Ogasawara N and Yokota A (2003) A functional link between RuBisCO-like protein of Bacillus and photosynthetic RuBisCO. Science 302:286–290

    Article  PubMed  CAS  Google Scholar 

  • Bamford VA, Bruno S, Rasmussen T, Appia-Ayme C, Cheesman MR, Berks BC and Hemmings AM (2002) Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme. EMBO J 21:5599–5610

    Article  PubMed  CAS  Google Scholar 

  • Beatty JT, Overmann J, Lince MT, Manske AK, Lang AS, Blankenship RE, Van Dover CL, Martinson TA and Plumley FG (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102:9306–9310

    Article  PubMed  CAS  Google Scholar 

  • Bias U and Trüper HG (1987) Species specific release of sulfate from adenylyl sulfate by ATP sulfurylase or ADP sulfurylase in the green sulfur bacteria Chlorobium limicola and Chlorobium vibrioforme. Arch Microbiol 147:406–410

    Article  CAS  Google Scholar 

  • Boone DR and Castenholz RW (2001) Bergey’s Manual of Systematic Bacteriology, 2nd edn., Vol 1, Springer, Berlin

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 847–870, Vol 2, of Advances in Photosynthesis (Govindjee ed.), Kluwer Academic (now Springer), Dordrecht

    Google Scholar 

  • Carrondo MA (2003) Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J 22: 1959–1968

    Article  PubMed  CAS  Google Scholar 

  • Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, Deuster O and Brune DC (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  PubMed  CAS  Google Scholar 

  • Dahl C (2008) Inorganic sulfur compounds as electron donors in purple sulfur bacteria. In: Hell R, Dahl C, Knaff DB, and Leustek T (eds) Sulfur Metabolism in Phototrophic Organisms, in press, Vol xxvii of Advances in Photosynthesis and Respiration (Govindjee ed.), Springer, New York

    Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA and Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514

    Article  PubMed  CAS  Google Scholar 

  • Friedrich CG, Rother D, Bardischewsky F, Quentmeier A and Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: Emergence of a common mechanism? Appl Environm Microbiol 67:2873–2882

    Article  CAS  Google Scholar 

  • Friedrich CG, Bardischewsky F, Rother D, Quentmeier A and Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259

    Article  PubMed  CAS  Google Scholar 

  • Frigaard N-U and Bryant DA (2004) Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria. Arch Microbiol 182: 265–276

    Article  PubMed  CAS  Google Scholar 

  • Frigaard N-U, Gomez Maqueo Chew A, Li H, Maresca JA and Bryant DA (2003) Chlorobium tepidum: Insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from the complete genome sequence. Photosynth Res 78: 93–117

    Article  PubMed  CAS  Google Scholar 

  • Frigaard N-U, Gomez Maqueo Chew A, Maresca JA and Bryant DA (2006) Bacteriochlorophyll biosynthesis in green bacteria. In: Grimm B, Porra R, Rüdiger W, and Scheer H (eds) Advances in Photosynthesis and Respiration, pp 201–221, Vol 25, Springer, Dordrecht

    Google Scholar 

  • Garrity GM and Holt JG (2001) Phylum BXI. Chlorobi phy. nov. In: Boone DR and Castenholz RW (eds) Bergey’s Manual of Systematic Bacteriology, 2nd edn., pp 601–623, Vol 1, Springer, New York

    Google Scholar 

  • Griesbeck C, Hauska G and Schütz M (2000) Biological sulfide oxidation: Sulfide-quinone reductase (SQR), the primary reaction. In: Pandalai SG (ed) Recent Research Developments in Microbiology, pp 179–203, Vol 4, Research Signpost, Trivandrum, India

    Google Scholar 

  • Griesbeck C, Schütz M, Schödl T, Bathe S, Nausch L, Mederer N, Vielreicher M and Hauska G (2002) Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565

    Article  PubMed  CAS  Google Scholar 

  • Hanson TE (2008) Proteome analysis of phototrophic sulfur bacteria with emphasis on sulfur metabolism. In: Hell R, Dahl C, Knaff DB and Leustek T (eds) Sulfur Metabolism in Phototrophic Organisms, in press, Vol xxvii of Advances in Photosynthesis and Respiration (Govindjee ed.), Springer, New York

    Google Scholar 

  • Hanson TE and Tabita FR (2001) A ribulose-1, 5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci USA 98:4397–4402

    Article  PubMed  CAS  Google Scholar 

  • Hanson TE and Tabita FR (2003) Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the Rubisco-like protein. Photosynth Res 78:231–248

    Article  PubMed  CAS  Google Scholar 

  • Heising S, Richter L, Ludwig W and Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain. Arch Microbiol 172:116–124

    Article  PubMed  CAS  Google Scholar 

  • Hensen D, Sperling D, Trüper HG, Brune DC and Dahl C (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Molec Microbiol, 62: 794–810

    Article  CAS  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. Intl J Syst Evol Microbiol 53:941–951

    Article  CAS  Google Scholar 

  • Imhoff JF (2008) Systematics of anoxygenic phototrophic bacteria. In: Hell R, Dahl C, Knaff DB and Leustek T (eds) Sulfur Metabolism in Phototrophic Organisms, in press, Vol xxvii of Advances in Photosynthesis and Respiration (Govindjee ed.), Springer, New York

    Google Scholar 

  • Kappler U and Dahl C (2001) Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203:1–9

    PubMed  CAS  Google Scholar 

  • Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG and Dahl C (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  PubMed  CAS  Google Scholar 

  • Khanna S and Nicholas DJD (1983) Substrate phosphorylation in Chlorobium vibrioforme f. sp. thiosulfatophilum. J Gen Microbiol 129:1365–1370

    CAS  Google Scholar 

  • Kirchhoff J and Trüper HG (1974) Adenylyl sulfate reductase of Chlorobium limicola. Arch Microbiol 100:115–120

    Article  CAS  Google Scholar 

  • Krafft T, Bokranz M, Klimmek O, Schroder I, Fahrenholz F, Kojro E and Kröger A (1992) Cloning and nucleotide-sequence of the psrA gene of Wolinella succinogenes polysulfide reductase. Eur J Biochem 206:503–510

    Article  PubMed  CAS  Google Scholar 

  • Kredich NM (1996) Biosynthesis of cysteine. In: Neidhardt FC (eds) Escherichia coli and Salmonella, 2nd edn., Vol 1, ASM

    Google Scholar 

  • Kumar S, Tamura K and Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings Bioinformatics 5:150–163

    Article  CAS  Google Scholar 

  • Lippert KD and Pfennig N (1969) Die Verwertung von molekularem Wasserstoff durch Chlorobium thiosulfatophilum. Arch Microbiol 65:29–47

    CAS  Google Scholar 

  • Ma KS, Weiss R and Adams MWW (2000) Characterization of hydrogenase II from the hyperthermophilic archaeon Pyrococcus furiosus and assessment of its role in sulfur reduction. J Bacteriol 182:1864–1871

    Article  PubMed  CAS  Google Scholar 

  • Manske AK, Glaeser J, Kuypers MAM and Overmann J (2005) Physiology and phylogeny of green sulfur bacteria forming a monospecific phototrophic assemblage at a depth of 100 meters in the Black Sea. Appl Environ Microbiol 71:8049–8060

    Article  PubMed  CAS  Google Scholar 

  • Méndez-Alvarez S, Pavón V, Esteve I, Guerrero R and Gaju N (1994) Transformation of Chlorobium limicola by a plasmid that confers the ability to utilize thiosulfate. J Bacteriol 176:7395–7397

    PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Neuwald AF, Krishnan BR, Brikun I, Kulakauskas S, Suziedelis K, Tomcsanyi T, Leyh TS and Berg DE (1992) cysQ, a gene needed for cysteine synthesis in Escherichia coli K-12 only during aerobic growth. J Bacteriol 174:415–425

    PubMed  CAS  Google Scholar 

  • Overmann J (2000) The family Chlorobiaceae. In: The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community, 3rd edn., release 3.1, Springer, New York, http://link.springer-ny.com/link/service/books/10125/

  • Overmann J (2008) Ecology of phototrophic sulfur bacteria. In: Hell R, Dahl C, Knaff DB, and Leustek T (eds) Advances in Photosynthesis and Respiration, Vol xxvii, Sulfur Metabolism in Phototrophic Organisms, in press, Springer, New York

    Google Scholar 

  • Overmann, J, Cypionka H and Pfennig N (1992) An extremely low-light-adapted phototrophic sulfur bacterium from the Black Sea. Limnol Oceanogr 37:150–155

    Article  CAS  Google Scholar 

  • Pires RH, Lourenco AI, Morais F, Teixeira M, Xavier AV, Saraiva LM and Pereira IAC (2003) A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta 1605:67–82

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Quentmeier A and 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  PubMed  CAS  Google Scholar 

  • Rákhely G, Kovács AT, Maróti G, Fodor BD, Csanádi G, Latinovics D and Kovács KL (2004) Cyanobacterial-type, heteropentameric, NAD+ -reducing NiFe hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 70: 722–728

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sander J, Engels-Schwarzlose S and 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  PubMed  CAS  Google Scholar 

  • Shahak Y, Arieli B, Padan E and Hauska G (1992) Sulfide quinone reductase (SQR) activity in Chlorobium. FEBS Lett 299:127–130

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Steinmetz MA and Fischer U (1982) Cytochromes, rubredoxin, and sulfur metabolism of the non-thiosulfate- utilizing green sulfur bacterium Pelodictyon luteolum. Arch Microbiol 132:204–210

    Article  Google Scholar 

  • Steinmetz MA and Fischer U (1985) Thiosulfate sulfur transferases (rhodaneses) of Chlorobium vibrioforme f. thiosulfatophilum. Arch Microbiol 142:253–258

    Article  CAS  Google Scholar 

  • Tabita F (1999) Microbial ribulose-1, 5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynth Res 60:1–28

    Article  CAS  Google Scholar 

  • Tamagnini P, Axelsson R, Lindberg, P, Oxelfelt, F, Wünschiers R and Lindblad P (2002) Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66:1–20

    Article  PubMed  CAS  Google Scholar 

  • Theissen U, Hoffmeister M, Grieshaber M and Martin W (2003) Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Molec Biol Evol 20:1564–1574

    Article  PubMed  CAS  Google Scholar 

  • Trüper HG and Pfennig N (1966) Sulphur metabolism in Thiorhodaceae. III. Storage and turnover of thiosulphate sulphur in Thiocapsa floridana and Chromatium species. Antonie van Leeuwenhoek 32:261–276

    Article  PubMed  Google Scholar 

  • Van Gemerden H and Mas J (1995) Ecology of phototrophic sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria, pp 49–85, Vol 2 of Advances in Photosynthesis (Govindjee, ed.), Kluwer Academic (now Springer), Dordrecht

    Google Scholar 

  • Verté F, Kostanjevecki V, De Smet L, Meyer TE, Cusanovich MA and Van Beeumen JJ (2002) Identification of a thiosulfate utilization gene cluster from the green phototrophic bacterium Chlorobium limicola. Biochemistry 41:2932–2945

    Article  PubMed  CAS  Google Scholar 

  • Vogl K, Glaeser J, Pfannes KR, Wanner G and Overmann J (2006) Chlorobium chlorochromatii sp. nov., a symbiotic green sulfur bacterium isolated from the phototrophic consortium “Chlorochromatium aggregatum”. Arch Microbiol 185: 363–372

    Article  PubMed  CAS  Google Scholar 

  • Ward DM, Ferris MJ, Nold SC and Bateson MM (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Molec Biol Rev 62:1353–1370

    CAS  Google Scholar 

  • Warthmann R, Cypionka H and Pfennig N (1992) Photoproduction of H2 from acetate by syntrophic cocultures of green sulfur bacteria and sulfur-reducing bacteria. Arch Microbiol 157:343–348

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Biology, University of Copenhagen, 2200, Copenhagen, Denmark

    Niels-Ulrik Frigaard

  2. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, 16802, University Park, PA, USA

    Donald A. Bryant

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  1. Niels-Ulrik Frigaard
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  2. Donald A. Bryant
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Editors and Affiliations

  1. University of Heidelberg, Im Neuenheimer Feld 360, 69120, Heidelberg, Germany

    Rüdiger Hell

  2. University of Bonn, Meckenheimer Allee 168, 53115, Bonn, Germany

    Christiane Dahl

  3. Texas Tech University, 79409-1061, Lubbock, TX, USA

    David Knaff

  4. Rutgers University, 59 Dudley Road, 08901-8520, New Brunswick, NJ, USA

    Thomas Leustek

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Frigaard, NU., Bryant, D.A. (2008). Genomic Insights into the Sulfur Metabolism of Phototrophic Green Sulfur Bacteria. In: Hell, R., Dahl, C., Knaff, D., Leustek, T. (eds) Sulfur Metabolism in Phototrophic Organisms. Advances in Photosynthesis and Respiration, vol 27. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6863-8_17

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