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Comparative and Functional Genomics of Anoxygenic Green Bacteria from the Taxa Chlorobi, Chloroflexi, and Acidobacteria

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Functional Genomics and Evolution of Photosynthetic Systems

Summary

Green bacteria are a diverse group of chlorophototrophic organisms belonging to three major taxa within the domain Bacteria: Chlorobi, Chloroflexi, and Acidobacteria. Most, although not all, of these organisms synthesize bacteriochlorophylls c, d or e and utilize chlorosomes for light harvesting. The pace of discoveries concerning the metabolism and physiology of these bacteria has accelerated rapidly since completion of the sequencing of the genomes of the green sulfur bacterium Chlorobaculum tepidum and the filamentous anoxygenic phototroph, Chloroflexus aurantiacus. This chapter summarizes insights gained from the extensive genome sequence data for members of these three taxa. The discovery of the first chlorophototrophic member of the phylum Acidobacteria, Candidatus Chloracidobacterium thermophilum, is also described, and recent insights into the physiology and metabolism of this unique, aerobic photoheterotroph are presented. Based upon phylogenetic inferences derived from analyses of sequences for reaction centers and enzymes of (bacterio)chlorophyll biosynthesis, some implications concerning the evolutionary origins of photosynthesis are discussed.

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Abbreviations

APS:

adenosine-5′-phosphosulfate

BChl:

bacteriochlorophyll

BChlide:

bacteriochlorophyllide

BPhe:

bacteriopheophytin

Cab. :

Chloracidobacterium

Cba. :

Chlorobaculum

Cfx. :

Chloroflexus

Chl. :

Chlorobium

Chl:

chlorophyll

Chlide:

chlorophyllide

Chp. :

Chloroherpeton

COG:

cluster of orthologous genes

COR:

chlorophyllide oxidoreductase

Cyt:

cytochrome

DPOR:

dark-operative protochlorophyllide oxidoreductase

DSR:

dissimilatory sulfite reductase

FAP:

filamentous anoxygenic phototroph

Fd:

ferredoxin

FMO:

Fenna-Matthews-Olson protein

FNR:

ferredoxin:NADP+oxidoreductase

GSB:

green sulfur bacterium/bacteria

H. :

Herpetosiphon

I. :

Ignavibacterium

O. :

Oscillochloris

ORF:

open reading frame

PAPS:

3′-phosphoadenosine-5′-phosphosulfate

PChlide:

protochlorophyllide

Phe:

pheophytin

Proto IX:

protoporphyrin IX

PSB:

purple sulfur bacteria

Ptc. :

Prosthecochloris

R. :

Roseiflexus

ROS:

reactive oxygen species

SAM:

S-adenosyl-L-methionine

SQR:

sulfide:quinone oxidoreductase

T. :

Thermomicrobium

References

  • Adhikari ND, Orler R, Chory J, Froehlich JE and Larkin RM (2009) Porphyrins promote the association of GENOMES UNCOUPLED 4 and a Mg-chelatase subunit with chloroplast membranes. J Biol Chem 284: 24783–24796

    PubMed  CAS  Google Scholar 

  • Alber BE and Fuchs G (2002) Propionyl-coenzyme A synthase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J Biol Chem 277: 12137–12143

    PubMed  CAS  Google Scholar 

  • Allewalt JP, Bateson MM, Revsbech NP, Slack K and Ward DM (2006) Effect of temperature and light on the growth of and photosynthesis by Synechococcus isolates typical of those predominating in the Octopus Spring microbial mat community of Yellowstone National Park. Environ Microbiol 72: 544–550

    CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410

    PubMed  CAS  Google Scholar 

  • Anderson KL, Tayne TA and Ward DM (1987) Formation and fate of fermentation products in hot spring cyanobacterial mats. Appl Environ Microbiol 53: 2343–2352

    PubMed  CAS  Google Scholar 

  • Arellano JB, Torkkeli M, Tuma R, Laurinmäki P, Melø TB, Ikonen TP, Butcher SJ, Serimaa RE and Pšenčík J (2008) Hexanol-induced order-disorder transitions in lamellar self-assembling aggregates of bacteriochlorophyll c in Chlorobium tepidum chlorosomes. Langmuir 24: 2035–2041

    PubMed  CAS  Google Scholar 

  • Azai C, Tsukatani Y, Harada J and Oh-oka H (2009) Sulfur oxidation in the mutants of the photosynthetic green ­sulfur bacterium Chlorobium tepidum devoid of cytochrome c-554 and SoxB. Photosynth Res 100: 57–65

    PubMed  CAS  Google Scholar 

  • Baniulis D, Yamashita E, Zhang H, Hasan SS and Cramer WA (2008) Structure-function of the cytochrome b 6       f complex. Photochem Photobiol 84: 1349–1358

    PubMed  CAS  Google Scholar 

  • Bateson MM and Ward DW (1988) Photoexcretion and fate of glycolate in a hot spring cyanobacterial mat. Appl Environ Microbiol 54: 1738–1743

    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

    PubMed  CAS  Google Scholar 

  • Ben Shem A, Frolow F and Nelson N (2004) Evolution of Photosystem I—from symmetry through pseudo-symmetry to asymmetry. FEBS Lett 564: 274–280

    PubMed  CAS  Google Scholar 

  • Berry EA, Huang S, Saechao LK, Pon NG, Valkova-Valchanova M and Daldal F (2004) X-ray structure of Rhodobacter capsulatus cytochrome bc 1: comparison with its mitochondrial and chloroplast counterparts. Photosynth Res 81: 251–275

    PubMed  CAS  Google Scholar 

  • Bhaya D, Grossman AR, Steunou AS, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Bateson MM, Ward DM and Heidelberg JF (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1: 703–713

    PubMed  CAS  Google Scholar 

  • Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33: 91–111

    PubMed  CAS  Google Scholar 

  • Blankenship RE, Feick R, Bruce BD, Kirmaier C, Holten D and Fuller RC (1983) Primary photochemistry in the facultative green photosynthetic bacterium Chloroflexus aurantiacus. J Cell Biochem 22: 251–261

    PubMed  CAS  Google Scholar 

  • Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B and Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453–1462

    PubMed  CAS  Google Scholar 

  • Bollivar DW (2006) Recent advances in chlorophyll biosynthesis. Photosynth Res 90: 173–194

    PubMed  CAS  Google Scholar 

  • Bollivar DW, Suzuki JY, Beatty JT, Dobrowolski JM and Bauer CE (1994) Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus. J Mol Biol 237: 622–640

    PubMed  CAS  Google Scholar 

  • Bröcker MJ, Virus S, Ganskow S, Heathcote P, Heinz DW, Schubert WD, Jahn D and Moser J (2008a) ATP-driven reduction by dark-operative protochlorophyllide oxidoreductase from Chlorobium tepidum mechanistically resembles nitrogenase catalysis. J Biol Chem 283: 10559–10567

    PubMed  Google Scholar 

  • Bröcker MJ, Wätzlich D, Uliczka F, Virus S, Saggu M, Lendzian F, Scheer H, Rüdiger W, Moser J and Jahn D (2008b) Substrate recognition of nitrogenase-like dark operative protochlorophyllide oxidoreductase from Prochlorococcus marinus. J Biol Chem 283: 29873–29881

    PubMed  Google Scholar 

  • Bröcker MJ, Schomburg S, Heinz DW, Jahn D, Schubert W-D and Moser J (2010) Crystal structure of the nitrogenase-like dark operative protochlorophyllide oxidoreductase catalytic complex (ChlN/ChlB)2. J Biol Chem 285: 27336–27345

    Google Scholar 

  • Bruce BD, Fuller RC and Blankenship RE (1982) Primary photochemistry in the facultatively aerobic green photosynthetic bacterium Chloroflexus aurantiacus. Proc Natl Acad Sci USA 79: 6532–6536

    PubMed  CAS  Google Scholar 

  • Brugna M, Albouy D and Nitschke W (1998) Diversity of cytochrome bc complexes: example of the Rieske protein in green sulfur bacteria. J Bacteriol 180: 3719–3723

    PubMed  CAS  Google Scholar 

  • Bryant DA and Frigaard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14: 488–496

    PubMed  CAS  Google Scholar 

  • Bryant DA, Vassilieva EV and Frigaard N-U (2002) Selective protein extraction from Chlorobium tepidum chlorosomes using detergents. Evidence that CsmA forms multimers and binds bacteriochlorophyll a. Biochemistry 41: 14403–14411

    PubMed  CAS  Google Scholar 

  • Bryant DA, Garcia Costas AM, Maresca JA, Chew AG, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF and Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317: 523–526

    PubMed  CAS  Google Scholar 

  • Buchanan BB and Arnon DI (1990) A reverse Krebs cycle in photosynthesis: consensus at last. Photosynth Res 24: 47–53

    PubMed  CAS  Google Scholar 

  • Burke DH, Alberti M and Hearst JE (1993a) The Rhodobacter capsulatus chlorin reductase-encoding locus, bchA, consists of three genes, bchX, bchY, and bchZ. J Bacteriol 175: 2407–2413

    PubMed  CAS  Google Scholar 

  • Burke DH, Alberti M and Hearst JE (1993b) bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants. J Bacteriol 175: 2414–2422

    PubMed  CAS  Google Scholar 

  • Caldwell PE, MacLean MR and Norris PR (2007) Ribulose bisphosphate carboxylase activity and a Calvin cycle gene cluster in Sulfobacillus species. Microbiology 153: 243–252

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Chung S, Frank G, Zuber H and Bryant DA (1994) Genes encoding two chlorosome components from the green sulfur bacterium Chlorobium vibrioforme strain 8327D and Chlorobium tepidum. Photosynth Res 41: 261–275

    CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B and Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311: 1283–1287

    PubMed  CAS  Google Scholar 

  • Coomber SA, Chaudhri M, Connor A, Britton G and Hunter CN (1990) Localized transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides. Mol Microbiol 4: 977–989

    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

    PubMed  CAS  Google Scholar 

  • Dahl C, Schulte A, Stockdreher Y, Hong C, Grimm F, Sander J, Kim R, Kim S-H and Shin DH (2008) Structural and molecular genetic insight into a widespread sulfur oxidation pathway. J Mol Biol 31: 1287–1300

    Google Scholar 

  • Davison PA, Schubert HL, Reid JD, Iorg CD, Heroux A, Hill CP and Hunter CN (2005) Structural and biochemical characterization of Gun4 suggests a mechanism for its role in chlorophyll biosynthesis. Biochemistry 44: 7603–7612

    PubMed  CAS  Google Scholar 

  • Diacovich L, Mitchell DL, Pham H, Gago G, Melgar MM, Khosla C, Gramajo H and Tsai SC (2004) Crystal structure of the beta-subunit of acyl-CoA carboxylase: structure-based engineering of substrate specificity. Biochemistry 43: 14027–14036

    PubMed  CAS  Google Scholar 

  • Ducluzeau AL, Chenu E, Capowiez L and Baymann F (2008) The Rieske/cytochrome b complex of Heliobacteria. Biochim Biophys Acta 1777: 1140–1146

    PubMed  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32: 1792–1797

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Feick RG and Fuller RC (1984) Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23: 3693–3700

    CAS  Google Scholar 

  • Feick RG, Fitzpatrick M and Fuller RC (1982) Isolation and characterization of cytoplasmic membranes and chlorosomes from the green bacterium Chloroflexus aurantiacus. J Bacteriol 150: 905–915

    PubMed  CAS  Google Scholar 

  • Feick R, Ertlmaier A and Ermler U (1996) Crystallization and X-ray analysis of the reaction center from the thermophilic green bacterium Chloroflexus aurantiacus. FEBS Lett 396: 161–164

    PubMed  CAS  Google Scholar 

  • Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA Merrick JM, McKenney K, Sutton G, FitzHugh W, Fields C, Gocayne JD, Scott J, Shirley R, Liu L-I, Glodek A, Kelley JM, Weidman JF, Phillips CA, Spriggs T, Hedblom E, Cotton MD, Utterback TR, Hanna MC, Nguyen DT, Saudek DM, Brandon RC, Fine LD, Fritchman JL, Fuhrmann JL, Geoghagen NSM, Gnehm, CL, McDonald LA, Small KV, Fraser CM, Smith HO and Venter JC (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496–512

    PubMed  CAS  Google Scholar 

  • Foster JM, Redlinger TE, Blankenship RE and Fuller RC (1986) Oxygen regulation of development of the photosynthetic membrane system in Chloroflexus aurantiacus. J Bacteriol 167: 655–659

    PubMed  CAS  Google Scholar 

  • Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman RD, Weidman JF, Small KV, Sandusky M, Fuhrmann J, Nguyen D, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb JF, Dougherty BA, Bott KF, Hu PC, Lucier TS, Peterson SN, Smith HO, Hutchison CA 3rd and Venter JC (1995) The minimal gene completement of Mycoplasma genitalium. Science 270: 397–403

    PubMed  CAS  Google Scholar 

  • Friedmann S, Alber BE and Fuchs G (2006a) Properties of succinyl-coenzyme A:L-malate coenzyme A transferase and its role in the autotrophic 3-hydroxypropionate cycle of Chloroflexus aurantiacus. J Bacteriol 188: 2646–2655

    PubMed  CAS  Google Scholar 

  • Friedmann S, Steindorf A, Alber BE and Fuchs G (2006b) Properties of succinyl-coenzyme A:D-citramalate coenzyme A transferase and its role in the autotrophic 3-hydroxypropionate cycle of Chloroflexus aurantiacus. J Bacteriol 188: 6460–6468

    PubMed  CAS  Google Scholar 

  • Friedmann S, Alber BE and Fuchs G (2007) Properties of R-citramalyl-coenzyme A lyase and its role in the autotrophic 3-hydroxypropionate cycle of Chloroflexus aurantiacus. J Bacteriol 189: 2906–2914

    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

    PubMed  CAS  Google Scholar 

  • Frigaard N-U and Bryant DA (2006) Chlorosomes: antenna organelles in green photosynthetic bacteria. In: Shively JM (ed) Complex Intracellular Structures in Prokaryotes, Microbiology Monographs, Vol 2, pp 79–114. Springer, Berlin

    Google Scholar 

  • Frigaard N-U and Bryant DA (2008a) Genomic insights into the sulfur metabolism of phototrophic sulfur bacteria. In: Hell R, Dahl C, Knaff DB and Leustek T (eds) Sulfur Metabolism in Phototrophic Organisms, pp 343–361. Springer, Dordrecht

    Google Scholar 

  • Frigaard N-U and Bryant DA (2008b) Genomic and evolutionary perspectives on sulfur metabolism in green sulfur bacteria. In: Friedrich CG and Dahl C (eds) Microbial Sulfur Metabolism (Proceedings of the International Symposium on Microbial Sulfur Metabolism), pp 60–76. Springer, Dordrecht

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frigaard N-U and Matsuura K (1999) Oxygen uncouples light absorption by the chlorosome antenna and photosynthetic electron transfer in the green sulfur bacterium Chlorobium tepidum. Biochim Biophys Acta 1412: 108–117

    Google Scholar 

  • Frigaard N-U, Voigt GD and Bryant DA (2002a) Chlorobium tepidum mutant lacking bacteriochlorophyll c made by inactivation of the bchK gene, encoding bacteriochlorophyll c synthase. J Bacteriol 184: 4358–4370

    Google Scholar 

  • Frigaard N-U, Vassilieva EV, Li H, Milks KJ, Zhao J and Bryant DA (2002b) The remarkable chlorosome. PS2001 Proceedings, Proceedings of the 12th International Congress on Photosynthesis, Brisbane, Australia. Article S1-003, CSIRO Publishing, Canberra, Australia

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frigaard N-U, Li H, Milks KJ and Bryant DA (2004a) Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. J Bacteriol 186: 646–653

    PubMed  CAS  Google Scholar 

  • Frigaard N-U, Maresca JA, Yunker CE, Jones AD and Bryant DA (2004b) Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 186: 5210–5220

    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 RJ, Rüdiger W and Scheer H (eds) Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications, pp 201–221. Springer, Dordrecht

    Google Scholar 

  • Fromme P, Jordan P and Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta 1507: 5–31

    PubMed  CAS  Google Scholar 

  • Fröstl JM and Overmann J (1998a) Physiology and tactic response of the phototrophic consortium “Chlorochromatium aggregatum.” Arch Microbiol 169: 129–135

    PubMed  Google Scholar 

  • Fröstl JM and Overmann J (1998b) Phylogenetic affiliation of the bacteria that constitute phototrophic consortia. Arch Microbiol 174: 50–58

    Google Scholar 

  • Fujita Y and Bauer CE (2000) Reconstitution of light-independent protochlorophyllide reductase from purified BchL and BchN-BchB subunits. In vitro confirmation of nitrogenase-like features of a bacteriochlorophyll biosynthesis enzyme. J Biol Chem 275: 23583–23588

    PubMed  CAS  Google Scholar 

  • Ganapathy S, Oostergetel GT, Wawrzyniak PK, Reus M, Gomez Maqueo Chew A, Buda F, Boekema EJ, Bryant DA, Holzwarth AR and de Groot HM (2009) Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc Natl Acad Sci USA 106: 8525–8530

    PubMed  CAS  Google Scholar 

  • Gao X, Xin Y and Blankenship RE (2009) Enzymatic activity of the alternative complex III as a menaquinol:auracyanin oxidoreductase in the electron transfer chain of Chloroflexus aurantiacus. FEBS Lett 583: 3275–3279

    PubMed  CAS  Google Scholar 

  • Garcia Costas AM, Liu Z, Tomsho LP, Schuster SC, Ward DM and Bryant DA (2011) Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based phototroph belonging to the phylum Acidobacteria. Environ Microbiol, accepted upon minor revision

    Google Scholar 

  • Garrity GM and Holt JG (2001) The road map to the Manual. In: Boone DR and Castenholz RW (eds) Bergey’s Manual of Systematic Bacteriology, 2nd Ed, Vol 1, pp 119–166. Springer, Berlin

    Google Scholar 

  • van Gemerden H and Mas J (1995) Ecology of phototrophic sulfur bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 49–85. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Gibson J, Pfennig N and Waterbury JB (1984) Chloroherpton thalassium gen. nov. et spec. nov., a non-filamentous, flexing and gliding green sulfur bacterium. Arch Microbiol 138: 96–101

    PubMed  CAS  Google Scholar 

  • Gich F, Airs RL, Danielsen M, Keely BJ, Abella CA, Garcia-Gil J, Miller M and Borrego CM (2003) Characterization of the chlorosome antenna of the filamentous anoxygenic phototrophic bacterium Chloronema sp. strain UdG9001. Arch Microbiol 180: 417–426

    PubMed  CAS  Google Scholar 

  • Giraud E and Verméglio A (2008) Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosynth Res 97: 141–153

    PubMed  CAS  Google Scholar 

  • Golbeck JH (1993) Shared thematic elements in photochemical reaction centers. Proc Natl Acad Sci USA 90: 1642–1646

    PubMed  CAS  Google Scholar 

  • Gomez Maqueo Chew A (2007) Elucidation of the bacteriochlorophyll c biosynthesis pathway in green sulfur bacterium Chlorobium tepidum. PhD thesis, The Pennsylvania State University, University Park, PA

    Google Scholar 

  • Gomez Maqueo Chew A and Bryant DA (2007a) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu Rev Microbiol 61: 113–129

    Google Scholar 

  • Gomez Maqueo Chew A and Bryant DA (2007b) Characterization of a plant-like protochlorophyllide a divinyl reductase in green sulfur bacteria. J Biol Chem 282: 2967–2975

    Google Scholar 

  • Gomez Maqueo Chew A, Frigaard N-U and Bryant DA (2007) Bacteriochlorophyllide c C-82 and C-121 methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J Bacteriol 189: 6176–6184

    PubMed  Google Scholar 

  • Gomez Maqueo Chew A, Frigaard N-U and Bryant DA (2009) Mutational analysis of three bchH paralogs in (bacterio-)chlorophyll biosynthesis in Chlorobaculum tepidum. Photosynth Res 101: 21–34

    PubMed  CAS  Google Scholar 

  • Graham JE and Bryant DA (2008) The biosynthetic pathway for synechoxanthin, an aromatic carotenoid synthesized by the euryhaline, unicellular cyanobacterium Synechococcus sp. strain PCC 7002. J Bacteriol 190: 7966–7974

    PubMed  CAS  Google Scholar 

  • Graham JE and Bryant DA (2009) The biosynthetic pathway for myxol-2′-fucoside (myxoxanthophyll) in the cyanobacterium Synechococcus sp. strain PCC 7002. J Bacteriol 191: 3292–3300

    PubMed  CAS  Google Scholar 

  • Granick S (1957) Speculations on the origins and evolution of photosynthesis. Ann NY Acad Sci 69: 292–308

    PubMed  CAS  Google Scholar 

  • Granick S (1965) Evolution of heme and chlorophyll. In: Bryson V and Vogel HG (eds), Evolving Genes and Proteins, pp 67–68. Academic Press, New York

    Google Scholar 

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

    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, Vol 4, pp 179–204. Research Signpost, Trivandrum

    Google Scholar 

  • Guindon S and Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. System Biol 52: 696–704

    Google Scholar 

  • Hager-Braun C, Xie DL, Jarosch U, Herold E, Büttner M, Zimmermann R, Deutzmann R, Hauska G and Nelson N (1995) Stable photobleaching of P840 in Chlorobium reaction center preparations: presence of the 42-kDa bacteriochlorophyll a protein and a 17-kDa polypeptide. Biochemistry 34: 9617–9624

    PubMed  CAS  Google Scholar 

  • Hanada S and Pierson BK (2006) The family Chloroflexaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H and Stackebrandt E (eds) The Prokaryotes, Vol 7, pp 815–842. Springer, Berlin

    Google Scholar 

  • Hanada S, Hiraishi A, Shimada K and Matsuura K (1995) Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement. Int J Syst Bacteriol 45: 676–681

    PubMed  CAS  Google Scholar 

  • Hanada S, Takaichi S, Matsuura K and Nakamura K (2002) Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int J Syst Evol Microbiol 52: 187–193

    PubMed  CAS  Google Scholar 

  • Harada J, Saga Y, Yaeda Y, Oh-oka H and Tamiaki H (2005) In vitro activity of C-20 methyltransferase, BchU, involved in bacteriochlorophyll c biosynthetic pathway in green sulfur bacteria. FEBS Lett 579: 1983–1987

    PubMed  CAS  Google Scholar 

  • Hauska G, Schoedle T, Remigy H and Tsiotis G (2001) The reaction center of green sulfur bacteria. Biochim Biophys Acta 1507: 260–277

    PubMed  CAS  Google Scholar 

  • Hegler F, Posth NR, Jiang J and Kappler A (2008) Physiology of phototrophic iron(II)-oxidizing bacteria: implications for modern and ancient environments. FEMS Microbiol Ecol 66: 250–260

    PubMed  CAS  Google Scholar 

  • Heinnickel M and Golbeck JH (2007) Heliobacterial photosynthesis. Photosynth Res 46: 2530–2536

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Herter S, Farfsing J, Gad’On N, Rieder C, Eisenreich W, Bacher A and Fuchs G (2001) Autotrophic CO2 fixation by Chloroflexus aurantiacus: study of glyoxylate formation and assimilation via the 3-hydroxypropionate cycle. J Bacteriol 183: 4305–4316

    PubMed  CAS  Google Scholar 

  • Herter S, Busch A and Fuchs G (2002a) L-Malyl-coenzyme A lyase/beta-methylmalyl-coenzyme A lyase from Chloroflexus aurantiacus, a bifunctional enzyme involved in autotrophic CO2 fixation. J Bacteriol 184: 5999–6006

    PubMed  CAS  Google Scholar 

  • Herter S, Fuchs G, Bacher A and Eisenreith W (2002b) A bicyclic autotrophic CO2 fixation pathway in Chloroflexus aurantiacus. J Biol Chem 277: 1501–1509

    Google Scholar 

  • Higuchi M, Hirano Y, Kimura Y, Oh-oka H, Miki K and Wang Z-Y (2009) Overexpression, characterization, and crystallization of the functional domain of cytochrome c z from Chlorobium tepidum. Photosynth Res 102: 77–84

    PubMed  CAS  Google Scholar 

  • Hillmann F, Fischer R-J, Saint-Prix F, Girbal L and Bahl H (2008) PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum. Mol Microbiol 68: 848–860

    PubMed  CAS  Google Scholar 

  • Hohmann-Marriott MF and Blankenship RE (2007) Variable fluorescence in green sulfur bacteria. Biochim Biophys Acta 1767: 106–113

    PubMed  CAS  Google Scholar 

  • Holkenbrink C, Ocón Barbas S, Mellerup A, Otaki H and Frigaard N-U (2011) Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system. Microbiology 157: 1229–1239

    Google Scholar 

  • Holt JG and Lewin RA (1968) Herpetosiphon aurantiacus gen. et sp. n., a new filamentous gliding organism. J Bacteriol 95: 2407–2408

    PubMed  CAS  Google Scholar 

  • Horimoto K, Fukuchi S and Mori K (2001) Comprehensive comparison between locations of orthologous genes on archaeal and bacterial genomes. Bioinformatics 17: 791–802

    PubMed  CAS  Google Scholar 

  • Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57: 55–77

    PubMed  Google Scholar 

  • Hugenholtz P and Stackebrandt E (2004) Reclassification of Sphaerobacter thermophilis from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia (emended description) in the phylum Chloroflexi (emended description). Int J Syst Evol Microbiol 54: 2049–2051

    PubMed  Google Scholar 

  • Hügler M, Menendez C, Schägger H and Fuchs G (2002) Malonyl-coenzyme A reductase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J Bacteriol 184: 2404–2410

    PubMed  Google Scholar 

  • Hügler M, Krieger RS, Jahn M and Fuchs G (2003) Characterization of acetyl-CoA/propioinyl-CoA carboxylase in Metallosphaera sedula. Carboxylating enzyme in the 3-hydroxypropionate cycle for autotrophic carbon fixation. Eur J Biochem 270: 736–744

    PubMed  Google Scholar 

  • Hügler M, Wirsen, CO, Fuchs G and Taylor CD, Sievert SM (2005) Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the ε subdivision of Proteobacteria. J Bacteriol 187: 3020–3027

    PubMed  Google Scholar 

  • Huster MS and Smith KM (1990) Biosynthetic studies of substituent homologation in bacteriochlorophylls c and d. Biochemistry 29: 4348–4355

    PubMed  CAS  Google Scholar 

  • Iino T, Mori K, Uchino Y, Nakagawa T, Harayama S and Suzuki KI (2010) Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestial hot spring, and proposal of Ignavibacteria classis nov. for a novel lineage at the periphery of the green sulfur bacteria. Int J Syst Evol Microbiol 60: 1376–1382

    PubMed  CAS  Google Scholar 

  • Ikonen TP, Li H, Pšenčík J, Laurinmaki PA, Butcher SJ Frigaard N-U, Serimaa RE, Bryant DA and Tuma R (2007) X-ray scattering and electron cryomicroscopy study on the effect of carotenoid biosynthesis to the structure of Chlorobium tepidum chlorosomes. Biophys J 93: 620–628

    PubMed  CAS  Google Scholar 

  • Imhoff JF (1995) Taxonomy and physiology of phototrophic purple bacteria and green sulfur bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 1–15. Kluwer Academic Publishers, Dordrecht

    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

    PubMed  CAS  Google Scholar 

  • Islam MR, Aikawa S, Midorikawa T, Kashino Y, Satoh K and Koike H (2008) Slr1923 of Synechocystis sp. PCC6803 is essential for conversion of 3,8-divinyl(protochlorophyll(ide) to 3-monovinyl(proto)chlorophyll(ide). Plant Physiol 148: 1068–1081

    PubMed  CAS  Google Scholar 

  • Ito H, Yokono M, Tanaka R and Tanaka A (2008) Identification of a novel vinyl reductase gene essential for the biosynthesis of monovinyl chlorophyll in Synechocystis sp. PCC 6803. J Biol Chem 283: 9002–9011

    PubMed  CAS  Google Scholar 

  • Ivanovsky RN, Fal YI, Berg IA, Ugolkova NV, Karsilnikova EN, Keppen OI, Zakharchuc LM and Zyakun AM (1999) Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium Oscillochloris triochoides strain DG-6. Microbiology 145: 1743–1748

    PubMed  CAS  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y and Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464: 1210–1213

    PubMed  CAS  Google Scholar 

  • Jackson TJ, Ramaley RF and Meinschein WG (1973) Thermomicrobium, a new genus of extremely thermophilic bacteria. Int J Syst Bacteriol 23: 28–36

    Google Scholar 

  • Jagannathan B and Golbeck JH (2008) Unifying principles in homodimeric type I photosynthetic reaction centers: properties of PscB and the FA, FB and FX iron clusters in green sulfur bacteria. Biochim Biophys Acta 1777: 1371–1380

    Google Scholar 

  • Jagannathan B and Golbeck JH (2009) Understanding of the binding interface between PsaC and the PsaA/PsaB heterodimer in Photosystem I. Biochemistry 48: 5405–5416

    PubMed  CAS  Google Scholar 

  • Johnson ET and Schmidt-Dannert C (2008) Characterization of three homologs of the large subunit of the magnesium chelatase from Chlorobaculum tepidum and interaction with the magnesium protoporphyrin IX methyltransferase. J Biol Chem 283: 27776–27784

    PubMed  CAS  Google Scholar 

  • Jurkevitch E (2007) Predatory behaviors in bacteria: diversity and transitions. Microbe 2: 67–73

    Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hisosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136 and 185–209

    PubMed  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M and Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8: 205–213, 227–253

    PubMed  CAS  Google Scholar 

  • Keppen OI, Tourova TP, Kuznetsov BB, Ivanovsky RN and Gorlenko VM (2000) Proposal of Oscillochloridaceae fam. Nov. on the basis of a phylogenetic analysis of the filamentous anoxygenic phototrophic bacteria, and emended description of Oscillochloris and Oscillochloris trichoides in comparison with further new isolates. Int J Syst Evol Microbiol 50: 1529–1537

    PubMed  Google Scholar 

  • Kiley PJ, Donohue TJ, Havelka WA and Kaplan S (1987) DNA sequence and in vitro expression of the B875 light-harvesting polypeptides of Rhodobacter sphaeroides. J Bacteriol 169: 742–750

    PubMed  CAS  Google Scholar 

  • Klappenbach JA and Pierson BK (2004) Phylogentic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium ‘Candidatus Chlorothrix halophila’ gen. nov., sp. nov., recovered from hypersaline microbial mats. Arch Microbiol 181: 17–25

    PubMed  CAS  Google Scholar 

  • Klatt CG, Bryant DA and Ward DM (2007) Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. Environ Microbiol 9: 2067–2078

    PubMed  CAS  Google Scholar 

  • Klatt CG, Wood JM, Rusch DB, Bateson MM, Hamamura N, Heidelberg JF, Grossman AR, Bhaya D, Cohan FM, Kühl M, Bryant DA and Ward DM (2011) Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J, in press

    Google Scholar 

  • Kondrat’eva EN and Krasil’nikova EN (1988) Utilization of thiosulfate by Chloroflexus aurantiacus. Mikrobiologiya (Eng transl) 57: 291–294

    Google Scholar 

  • Krasil’nikova EN (1987) ATP sulfurylase activity in Chloroflexus aurantiacus and other photosynthesizing bacteria as a function of temperature. Mikrobiologiya (Eng transl) 55: 418–421

    Google Scholar 

  • Krasil’nikova EN and Kondrat’eva EN (1987) Growth of Chloroflexus aurantiacus under anaerobic conditions in the dark and the metabolism of organic substrates. Mikrobiologiya (Eng transl) 56: 281–285

    Google Scholar 

  • Krügel H, Krubasik P, Weber K, Saluz HP and Sandmann G (1999) Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim Biophys Acta 1439: 57–64

    PubMed  Google Scholar 

  • Kurtz DM Jr (2006) Avoiding high valent iron intermediates: superoxide reductase and rubrerythrin. J Inorg Biochem 100: 679–693

    PubMed  CAS  Google Scholar 

  • Kuznetsov BB, Ivanovsky RN, Keppen OI, Sukhacheva MV, Bumazhkin BK, Patutina EO, Beletsky AV, Mardanov AV, Baselerov RV, Panteleeva AN, Kolganova TV, Ravin NV and Skryabin KG (2011) Draft genome sequence of the anoxygenic filamentous phototrophic bacterium Oscillochloris trichoides DG-6. J Bacteriol 193: 321–322

    Google Scholar 

  • Layer G, Kervio E, Morlock G, Heinz DW, Jahn D, Retey J and Schubert WD (2005) Structural and functional comparison of HemN to other radical SAM enzymes. Biol Chem 386: 971–980

    PubMed  CAS  Google Scholar 

  • Lebrun E, Brugna M, Baymann F, Muller D, Lièvremont D, Lett M-C and Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20: 686–693

    PubMed  CAS  Google Scholar 

  • Lee M, del Rosario MC, Harris HH, Blankenship RE, Guss JM and Freeman HC (2009a) The crystal structure of auracyanin A at 1.85  Å resolution: the structures and functions of auracyanins A and B, two almost identical “blue” copper proteins, in the photosynthetic bacterium Chloroflexus aurantiacus. J Biol Inorg Chem 14: 329–345

    PubMed  CAS  Google Scholar 

  • Lee ZM, Bussema C 3rd and Schmidt TM (2009b) rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucl Acids Res 37: D489–493

    PubMed  CAS  Google Scholar 

  • Lehmann RP, Brunisholz RA and Zuber H (1994) Structural differences in chlorosomes of Chloroflexus aurantiacus grown under different conditions support the BChl c-binding function of the 5.7 kDa protein. FEBS Lett 342: 319–324

    PubMed  CAS  Google Scholar 

  • Li H (2006) Organization and function of chlorosome proteins in the green sulfur bacterium Chlorobium tepidum. PhD thesis, The Pennsylvania State University, University Park, PA

    Google Scholar 

  • Li H and Bryant DA (2009) Envelope proteins of the CsmB/CsmF and CsmC/CsmD motif families influence the size, shape, and composition of chlorosomes in Chlorobaculum tepidum. J Bacteriol 191: 7109–7120

    PubMed  CAS  Google Scholar 

  • Li H, Frigaard N-U and Bryant DA (2006) Molecular contacts for chlorosome envelope proteins revealed by cross-linking studies with chlorosomes from Chlorobium tepidum. Biochemistry 45: 9095–9103

    PubMed  CAS  Google Scholar 

  • Li H, Jubelirer S, Garcia Costas AM, Frigaard N-U and Bryant DA (2009) Multiple antioxidant proteins protect Chlorobaculum tepidum against oxygen and reactive oxygen species. Arch Microbiol 191: 853–867

    PubMed  CAS  Google Scholar 

  • Li L, Stoeckert CJ Jr and Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189

    PubMed  CAS  Google Scholar 

  • Lippert K-D and Pfennig N (1969) Die Verwertung von molecularem Wasserstoff durch Chlorobium thiosulfatophilum. Arch Microbiol 65: 29–47

    CAS  Google Scholar 

  • Liu Z and Bryant DA (2011) Identification of a gene essential for the first committed step in the biosynthesis of bacteriochlorophyll c. J Biol Chem 286: 22393–22402

    Google Scholar 

  • Liu Z, Klatt CG, Wood JM, Rusch DB, Ludwig M, Wittekindt N, Tomsho LP, Schuster SC, Ward DM and Bryant DA (2011) Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J, in press

    Google Scholar 

  • Ludwig W and Klenk H-P (2001) Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. In: Boone DR and Castenholz RW (eds) Bergey’s Manual of Systematic Bacteriology, 2nd Ed, Vol 1, pp 49–65. Springer, Berlin

    Google Scholar 

  • Madigan MT, Petersen SR and Brock TD (1974) Nutritional studies on Chloroflexus, a filamentous photosynthetic, gliding bacterium. Arch Microbiol 100: 97–103

    CAS  Google Scholar 

  • Madigan MT and Brock T (1977a) Photosynthetic sulfide oxidation by Chloroflexus aurantiacus, a filamentous, photosynthetic, gliding bacterium. J Bacteriol 122: 782–784

    Google Scholar 

  • Madigan MT and Brock TD (1977b) ‘Chlorobium-type’ vesicles of photosynthetically-grown Chloroflexus aurantiacus observed using negative staining techniques. J Gen Microbiol 102: 279–285

    Google Scholar 

  • Manske AK, Glaeser J, Kuypers MM and Overmann J (2006) 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

    Google Scholar 

  • Marcia M, Ermler U, Peng G and Michel H (2009) The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc Natl Acad Sci USA 106: 9625–9630

    PubMed  CAS  Google Scholar 

  • Maresca JA and Bryant DA (2006) Two genes encoding new carotenoid-modifying enzymes in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 188: 6217–6223

    PubMed  CAS  Google Scholar 

  • Maresca JA, Gomez Maqueo Chew A, Ponsatí MR, Frigaard N-U, Ormerod JG and Bryant DA (2004) The bchU gene of Chlorobium tepidum encodes the C-20 methyltransferase in bacteriochlorophyll c-biosynthesis. J Bacteriol 186: 2558–2566

    PubMed  CAS  Google Scholar 

  • Maresca JA, Graham JE, Wu M, Eisen JA and Bryant DA (2007) Identification of a fourth family of lycopene cyclases in photosynthetic bacteria. Proc Natl Acad Sci USA 104: 11784–11789

    Google Scholar 

  • Maresca JA, Romberger SP and Bryant DA (2008a) Isorenieratene biosynthesis in green sulfur bacteria requires the cooperative actions of two carotenoid cyclases. J Bacteriol 190: 6384–6391

    PubMed  CAS  Google Scholar 

  • Maresca JA, Graham JE and Bryant DA (2008b) The biochemical basis for structural diversity in the carotenoids of chlorophototrophic bacteria. Photosynth Res 97: 121–140

    PubMed  CAS  Google Scholar 

  • van der Meer MTJ, Schouten S, de Leeuw JW and Ward DM (2000) Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopically heavy organic carbon in the geological record. Environ Microbiol 2: 428–435

    PubMed  Google Scholar 

  • van der Meer MTJ, Schouten S, Bateson MM, Nübel U, Wieland A, Kühl M, de Leeuw JW, Sinninghe Damsté JS and Ward DM (2005) Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone National Park. Appl Environ Microbiol 71: 3978–3986

    PubMed  Google Scholar 

  • van der Meer MTJ, Klatt CG, Wood J, Bryant DA, Bateson MM, Lammerts L, Schouten S, Sinninghe Damsté JS, Madigan MT and Ward DM (2010) Cultivation and genomic, nutritional and lipid biomarker characterization of Roseiflexus sp. strains closely related to predominant in situ populations inhabiting Yellowstone hot spring microbial mats. J Bacteriol 192: 3033–3042

    PubMed  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 

  • Méndez-Alvarez S, Pavón V, Esteve I, Guerrero R and Gaju N (1995) Genomic heterogeneity in Chlorobium limicola: chromosomic and plasmidic differences among strains. FEMS Microbiol Lett 134: 279–285

    PubMed  Google Scholar 

  • Meyer TE (1994) Evolution of photosynthetic reaction centers and light harvesting chlorophyll proteins. BioSystems 33: 165–175

    Google Scholar 

  • Mi H, Endo T, Ogawa T and Asada K (1995) Thylakoid membrane-bound NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36: 661–668

    CAS  Google Scholar 

  • Milks KJ, Danielsen M, Persson S, Jensen ON, Cox RP and Miller M (2005) Chlorosome proteins studied by MALDI-TOF-MS: topology of CsmA in Chlorobium tepidum. Photosynth Res 86: 113–121

    PubMed  CAS  Google Scholar 

  • Mix LJ, Haig D and Cavanaugh CM (2005) Phylogenetic analyses of the core antenna domain: investigating the origin of photosystem I. J Mol Evol 60: 153–163

    PubMed  CAS  Google Scholar 

  • Montaño GA, Wu HM, Lin S, Brune DC and Blankenship RE (2003) Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42: 10246–10251

    PubMed  Google Scholar 

  • Mulkidjanian AY (2007) Proton translocation by the cytochrome bc 1 complexes of phototrophic bacteria: introducing the activated Q-cycle. Photochem Photobiol Sci 6: 19–34

    PubMed  CAS  Google Scholar 

  • Mulkidjanian AY and Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis. A primordial UV-protector as common ancestor of reaction centers and antenna proteins. Photosynth Res 51: 27–42

    CAS  Google Scholar 

  • Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A, Partensky F, Burd H, Kaznadzey D, Haselkorn R and Galperin MY (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 103: 13126–13131

    PubMed  CAS  Google Scholar 

  • Muraki N, Seo D, Shiba T, Sakurai T and Kurisu G (2008) Crystallization and preliminary X-ray studies of ferredoxin-NAD(P)+ reductase from Chlorobium tepidum. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 186–189

    PubMed  Google Scholar 

  • Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H, Kurisu G and Fujita Y (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465: 110–114

    PubMed  CAS  Google Scholar 

  • Nadson GA (1906) The morphology of inferior algae. III. Chlorobium limicola Nads., the green chlorophyll bearing microbe. Bull Jard Bot St Petersb 6: 190

    Google Scholar 

  • Nagata N, Tanaka R, Satoh S and Tanaka A (2005) Identification of a vinyl reductase gene for chlorophyll biosynthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17: 233–240

    PubMed  CAS  Google Scholar 

  • Nagata N, Tanaka R and Tanaka A (2007) The major route for chlorophyll synthesis include [3,8-divinyl]-chlorophyllide a reduction in Arabidopsis thaliana. Plant Cell Physiol 48: 1803–1808

    PubMed  CAS  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M and Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 9: 123–130

    PubMed  CAS  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Takeuchi C, Yamada M and Tabata S (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10: 137–145

    PubMed  CAS  Google Scholar 

  • Niedermeier G, Shiozawa JA, Lottspeich F and Feick RG (1994) The primary structure of two chlorosome proteins from Chloroflexus aurantiacus. FEBS Lett 342: 61–65

    PubMed  CAS  Google Scholar 

  • Nisbet EG, Cann JR and Van Dover CL (1995) Did photosynthesis begin from thermotaxis? Nature 373: 479–480

    CAS  Google Scholar 

  • Nomata J, Swem LR, Bauer CE and Fujita Y (2005) Over­expression and characterization of dark-operative ­protochlorophyllide reductase from Rhodobacter capsulatus. Biochim Biophys Acta 1708: 229–237

    PubMed  CAS  Google Scholar 

  • Nomata J, Mizoguchi T, Tamiaki H and Fujita Y (2006) A second nitrogenase-like enzyme for bacteriochlorophyll biosynthesis: reconstitution of chlorophyllide a reductase with purified X-protein (BchX) and YZ-protein (BchY-BchZ) from Rhodobacter capsulatus. J Biol Chem 281: 15021–15028

    PubMed  CAS  Google Scholar 

  • Nomata J, Ogawa T, Kitashima M, Inoue K and Fujita Y (2008) NB-protein (BchN-BchB) of dark-operative protochlorophyllide reductase is the catalytic component containing oxygen-tolerant Fe-S clusters. FEBS Lett 582: 1346–1350

    PubMed  CAS  Google Scholar 

  • Oelze J (1992) Light and oxygen regulation of the synthesis of bacteriochlorophylls a and c in Chloroflexus aurantiacus. J Bacteriol 172: 5021–5026

    Google Scholar 

  • Ogawa T, Furusawa T, Nomura R, Seo D, Hosoya-Matsuda N, Sakurai H and Inoue K (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

    PubMed  CAS  Google Scholar 

  • Ohashi S, Miyashita H, Okada N, Iemura T, Watanabe T and Kobayashi M (2008) Unique photosystems in Acaryochloris marina. Photosynth Res 98: 141–149

    PubMed  CAS  Google Scholar 

  • Oh-oka H, Kamei S, Matsubara H, Iwaki M and Itoh S (1995) Two molecules of cytochrome c function as the electron donors to P840 in the reaction center complex isolated from a green sulfur bacterium Chlorobium tepidum. FEBS Lett 365: 30–24

    PubMed  CAS  Google Scholar 

  • Oh-oka H, Iwaki M and Itoh S (1997) Vicosity dependence of the electron transfer rate from bound cytochrome c to P840 in the photosynthetic reaction center of the green sulfur bacterium Chlorobium tepidum. Biochemistry 36: 9267–9272

    PubMed  CAS  Google Scholar 

  • Oh-oka H, Iwaki M and Itoh S (1998) Membrane-bound cytochrome c z couples quinol oxidoreductase to the P840 reaction center complex in isolated membranes of the green sulfur bacterium Chlorobium tepidum. Biochemistry 37: 12293–12300

    PubMed  CAS  Google Scholar 

  • Okkels JS, Kjær B, Hansson O, Svendsen I, Møller BL and Scheller HV (1992) A membrane-bound monoheme cytochrome c 551 of a novel type is the immediate electron donor to P840 of the Chlorobium vibrioforme photosynthetic reaction center complex. J Biol Chem 267: 21139–21145

    PubMed  CAS  Google Scholar 

  • Olson JM (1999) Early evolution of chlorophyll-based photosystems. Biochem Molec Biol 12: 468–482

    CAS  Google Scholar 

  • Olson JM and Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80: 373–386

    PubMed  CAS  Google Scholar 

  • Olson JM and Pierson BK (1987) Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol 108: 209–248

    PubMed  CAS  Google Scholar 

  • Oostergetel GT, Reus M, Gomez Maqueo Chew A, Bryant DA, Boekema EJ and Holzwarth AR (2007) Long-range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryo-electron microscopy. FEBS Lett 581: 5435–5439

    PubMed  CAS  Google Scholar 

  • Oostergetel GT, van Amerongen H and Boekema EJ (2010) The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth Res 104: 245–255

    PubMed  CAS  Google Scholar 

  • Ouchane S, Stenou AS, Picaud M and Astier C (2004) Aerobic and anaerobic Mg-protoporphyrin monomethyl ester cyclases in purple bacteria: a strategy adopted to bypass the repressive oxygen control system. J Biol Chem 279: 6385–6394

    PubMed  CAS  Google Scholar 

  • Overmann J (1997) Mahoney Lake: a case study of the ecological significance of phototrophic sulfur bacteria. Adv Microbial Ecol 15: 251–288

    CAS  Google Scholar 

  • Overmann J (2001) Green sulfur bacteria. In: Boone DR and Castenholz RW (eds) Bergey’s Manual of Systematic Bacteriology, 2nd Ed, Vol 1, pp 601–605. Springer, Berlin

    Google Scholar 

  • Overmann J (2006) Green sulfur bacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H and Stackebrandt E (eds) The Prokaryotes, Vol 7, pp 359–378. Springer, Berlin

    Google Scholar 

  • Overmann J and Tuschak C (1997) Phylogeny and molecular fingerprinting of green sulfur bacteria. Arch Microbiol 167: 302–309

    PubMed  CAS  Google Scholar 

  • Pedersen MØ, Borch J, Højrup P and Cox RP, Miller M (2007) The light-harvesting antenna of Chlorobium tepidum: interactions between the FMO protein and the major chlorosome protein CsmA studied by surface plasmon resonance. Photosynth Res 89: 63–69

    Google Scholar 

  • Pedersen MØ, Pham, L, Steensgaard DB and Miller M (2008a) A reconstituted light-harvesting complex from the green sulfur bacterium Chlorobium tepidum containing CsmA and bacteriochlorophyll a. Biochemistry 47: 1435–1441

    PubMed  CAS  Google Scholar 

  • Pedersen MØ, Underhaug J, Dittmer J, Miller M and Nielsen NC (2008b) The three dimensional structure of CsmA: a small antenna protein from the green sulfur bacterium Chlorobium tepidum. FEBS Lett 582: 2869–2874

    PubMed  CAS  Google Scholar 

  • Pedersen MØ, Linnanto J, Frigaard N-U, Nielsen NC and Miller M (2010) A model of the protein-pigment baseplate complex in chlorosomes. Photosynth Res 104: 233–243

    PubMed  CAS  Google Scholar 

  • Pereira MM, Refojo PN, Hreggvidsson GO, Hjorleifsdottir S and Teixeira M (2007) The alternative complex III from Rhodothermus marinus – a prototype of a new family of quinol:electron acceptor oxidoreductases. FEBS Lett 581: 4831–4835

    PubMed  CAS  Google Scholar 

  • Phadwal K (2005) Carotenoid biosynthetic pathway: molecular phylogenies and evolutionary behavior of crt genes in eubacteria. Gene 345: 35–43

    PubMed  CAS  Google Scholar 

  • Pierson BK and Castenholz RW (1974) A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100: 5–24

    PubMed  CAS  Google Scholar 

  • Pierson BK and Thornber JP (1983) Isolation and spectral characterization of photochemical reaction centers from the thermophilic green bacterium Chloroflexus aurantiacus strain J-10-fl. Proc Natl Acad Sci USA 80: 80–84

    PubMed  CAS  Google Scholar 

  • Pierson BK, Giovannoni SJ, Stahl DA and Castenholz RW (1985) Heliothrix oregonensis, gen. nov., sp. nov., a phototrophic filamentous bacterium containing bacteriochlorophyll a. Arch Microbiol 142: 164–167

    PubMed  CAS  Google Scholar 

  • Pinta V, Picaud M, Reiss-Husson F and Astier C (2002) Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J Bacteriol 184: 746–753

    PubMed  CAS  Google Scholar 

  • Pšenčík J, Ikonen TP, Laurinmäki P, Merckel MC, Butcher SJ, Serimaa RE and Tuma R (2004) Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys J 87: 1165–1172

    PubMed  Google Scholar 

  • Pšenčík J, Arellano JB, Ikonen TP, Borrego CM, Laurinmäki PA, Butcher SJ, Serimaa RE and Tuma R (2006) Internal structure of chlorosomes from brown-colored Chlorobium species and the role of carotenoids in their assembly. Biophys J 91: 1433–1440

    PubMed  Google Scholar 

  • Pšenčík J, Collins AM, Liljeroos L, Torkkeli M, Laurinmäki P, Ansink HM, Ikonen TP, Serimaa RE, Blankenship RE, Tuma R and Butcher SJ (2009) Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J Bacteriol 191: 6701–6708

    PubMed  Google Scholar 

  • Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY and Blankenship RE (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298: 1616–1620

    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

    PubMed  CAS  Google Scholar 

  • Sadekar S, Raymond J and Blankenship RE (2006) Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. Mol Biol Evol 23: 2001–2007

    PubMed  CAS  Google Scholar 

  • Saga Y and Tamiaki H (2006) Transmission electron microscopic study on supramolecular nanostructures of bacteriochlorophyll self-aggregates in chlorosomes of green photosynthetic bacteria. J Biosci Bioeng 102: 118–123

    PubMed  CAS  Google Scholar 

  • Sakuragi Y, Frigaard N-U, Shimada K and Matsuura K (1999) Association of bacteriochlorophyll a with the CsmA protein in chlorosomes of the photosynthetic green filamentous bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 1413: 172–180

    PubMed  CAS  Google Scholar 

  • Sandmann G (2009) Evolution of carotene desaturation: the complication of a simple pathway. Arch Biochem Biophys 483: 169–174

    PubMed  CAS  Google Scholar 

  • Sarma R, Barney BM, Hamilton TL, Jones A, Seefeldt LC and Peters JW (2008) Crystal structure of the L protein of Rhodobacter sphaeroides light-independent protochlorophyllide reductase with MgADP bound: a homologue of the nitrogenase Fe protein. Biochemistry 47: 13004–13015

    PubMed  CAS  Google Scholar 

  • Schmidt S, Biegel E and Müller V (2009) The ins and outs of Na+ bioenergetics in Acetobacterium woodii. Biochim Biophys Acta 1787: 691–696

    PubMed  CAS  Google Scholar 

  • Schubert W-D, Klukas O, Saenger W, Witt HT, Fromme P and Krauß N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J Mol Biol 280: 297–314

    PubMed  CAS  Google Scholar 

  • Schütz M, Zirnbigl S, le Coutre J, Büttner M, Xie D-L, Nelson N, Deutzmann R and Hauska G (1994) A transcription unit for the Rieske FeS-protein and cytochrome b in Chlorobium limicola. Photosynth Res 39: 163–174

    Google Scholar 

  • Schütz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter KO, Hauska G, Toci R, Lemesle-Meunier D, Tron P, Schmidt C and Nitschke W (2000) Early evolution of cytochrome bc complexes. J Mol Biol 300: 663–675

    PubMed  Google Scholar 

  • Sekiguchi Y, Yamada T, Hanada S, Ohashi A, Harada H and Kamagata Y (2003) Anaerolinea thermophila gen. nov., sp. nov. and Caldilinea aerophila gen. nov., sp. nov., novel filamentous thermophiles that represent a previously uncultured lineage of the domain Bacteria at the subphylum level. Int J Syst Evol Microbiol 53: 1843–1851

    PubMed  CAS  Google Scholar 

  • Seo D and Sakurai H (2002) Purification and characterization of ferredoxin-NAD(P)+ reductase from the green sulfur bacterium Chlorobium tepidum. Biochim Biophys Acta 1597: 123–132

    PubMed  CAS  Google Scholar 

  • Seo D, Tomioka A, Kusumoto N, Kamo M, Enami I and Sakurai H (2001) Purification of ferredoxins and their reaction with purified reaction center complex from the green sulfur bacterium Chlorobium tepidum. Biochim Biophys Acta 1503: 377–384

    PubMed  CAS  Google Scholar 

  • Seshadri R, Adrian L, Fouts DE, Eisen JA, Phillippy AM, Methe BA, Ward NL, Nelson WC, Deboy RT, Khouri HM, Kolonay JF, Dodson RJ, Daugherty SC, Brinkac LM, Sullivan SA, Madupu R, Nelson KE, Kang KH, Impraim M, Tran K, Robinson JM, Forberger HA, Fraser CM, Zinder SH and Heidelberg JF (2005) Genome sequence of the PCE-dechlorinating bacterium Dehalococcoides ethenogenes. Science 307: 105–108

    PubMed  CAS  Google Scholar 

  • Shioi Y, Watanabe K and Takamiya K (1996) Enzymatic conversion of pheophorbide a to a precursor of pyropheophorbide a in leaves of Chenopodium album. Plant Cell Physiol 37: 1143–1149

    CAS  Google Scholar 

  • Shiozawa JA, Lottspeich F and Feick R (1987) The photochemical reaction center of Chloroflexus aurantiacus is composed of two structurally similar polypeptides. Eur J Biochem 167: 595–600

    Google Scholar 

  • Shiozawa JA, Lottspeich F and Feick R (1989) The primary structure of the Chloroflexus aurantiacus reaction-center polypeptides. Eur J Biochem 180: 75–84

    PubMed  CAS  Google Scholar 

  • Sirevåg R (1995) Carbon metabolism in green bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 871–883. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Sirevåg R and Castenholz RW (1979) Aspects of car­bon metabolism in Chloroflexus. Arch Microbiol 120:151–153

    Google Scholar 

  • Sobotka R, Dühring U, Komenda J, Peter E, Gardian Z, Tichy M, Grimm B and Wilde A (2008) Importance of the cyanobacterial Gun4 protein for chlorophyll metabolism and assembly of photosynthetic complexes. J Biol Chem 283: 25794–25802

    PubMed  CAS  Google Scholar 

  • Sørensen PG, Cox RP and Miller M (2008) Chlorosome lipids from Chlorobium tepidum: characterization and quantification of polar lipids and wax esters. Photosynth Res 95: 191–196

    PubMed  Google Scholar 

  • Staehelin LA, Golecki JR and Drews G (1980) Supermolecular Organization of chlorosomes (Chlorobium vesicles) and of their membrane attachment sites. Biochim Biophys Acta 589: 30–45

    PubMed  CAS  Google Scholar 

  • Sprague SG, Staehelin LA, DiBartolomeis MJ and Fuller RC (1981) Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus. J Bacteriol 147: 1021–1031

    PubMed  CAS  Google Scholar 

  • Steuber J (2001) Na+ translocation by bacterial NADH:quinone oxidoreductases: an extension to the complex-I family of primary redox pumps. Biochim Biophys Acta 1505: 45–56

    PubMed  CAS  Google Scholar 

  • Strauss G and Fuchs G (1993) Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur J Biochem 215: 633–643

    PubMed  CAS  Google Scholar 

  • Suzuki JY and Bauer CE (1995) Altered monovinyl and divinyl protochlorophyllide pools in bchJ mutants of Rhodobacter capsulatus. Possible monovinyl substrate discrimination of light-independent protochlorophyllide reductase. J Biol Chem 270: 3732–3740

    PubMed  CAS  Google Scholar 

  • Suzuki JY, Bollivar DW and Bauer CE (1997) Genetic ana­lysis of chlorophyll biosynthesis. Annu Rev Genet 31: 61–89

    PubMed  CAS  Google Scholar 

  • Swartz TH, Ikewada S, Ishikawa O, Ito M and Krulwich TA (2005) The Mrp system: a giant among monovalent cation/proton antiporters? Extremophiles 9: 345–354

    PubMed  CAS  Google Scholar 

  • Swingley WD, Sadekar S, Mastrian SD, Matthies JH, Hao J, Ramos H, Acharya CR, Conrad AL, Taylor HL, Dejesa LC, Shah MK, O’huallachain ME, Lince MT, Blankenship RE, Beatty JT and Touchman JW (2007) The complete genome sequence of Roseobacter denitrificans reveals a mixotrophic rather than photosynthetic metabolism. J Bacteriol 189: 683–690

    PubMed  CAS  Google Scholar 

  • Tabita FR (2009) The hydroxypropionate pathway of CO2 fixation: fait accompli. Proc Natl Acad Sci USA 106: 21015–21016

    PubMed  CAS  Google Scholar 

  • Taisova AS, Keppen OI, Lukashev EP, Arutyunyan AM and Fetisova Z (2002) Study of the chlorosomal antenna of the green mesophilic filamentous bacterium Oscillochloris trichoides. Photosynth Res 74: 73–85

    PubMed  CAS  Google Scholar 

  • Takaichi S (2001) Carotenoids and carotenogenesis in anoxygenic photosynthetic bacteria. In: Frank HA, Young AJ, Britton G and Cogdell RJ (eds) The Photochemistry of Carotenoids, pp 39–69. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Tamura K, Dudley J, Nei M and Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599

    PubMed  CAS  Google Scholar 

  • Tanaka R and Tanaka A (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9: 248–255

    PubMed  CAS  Google Scholar 

  • Tanaka R and Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321–346

    PubMed  CAS  Google Scholar 

  • Tang KH, Wen J, Li X and Blankenship RE (2009) Role of the AcsF protein in Chloroflexus aurantiacus. J Bacteriol 191: 3580–3587

    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. Mol Biol Evol 20: 1564–1574

    PubMed  CAS  Google Scholar 

  • Theroux SJ, Redlinger TE, Fuller RC and Robinson SJ (1990) Gene encoding the 5.7 kilodalton chlorosome protein of Chloroflexus aurantiacus: Regulated message levels and a predicted carboxy-terminal protein extension. J Bacteriol 172: 4497–4504

    PubMed  CAS  Google Scholar 

  • Tiller ERM and Collins RA (2000) Genome rearrangement by replication-directed translocation. Nat Genet 26: 195–197

    Google Scholar 

  • Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, Podar M, Short JM, Mather EJ, Detter JC, Bork P, Hugenholtz P and Rubin EM (2005) Comparative metagenomics of microbial communities. Science 308: 554–557

    PubMed  CAS  Google Scholar 

  • Tronrud DE, Wen J, Gay L and Blankenship RE (2009) The structural difference in absorption spectra for the FMO protein from green sulfur bacteria. Photosynth Res 100: 79–87

    PubMed  CAS  Google Scholar 

  • Tsukatani Y, Miyamoto R, Itoh S and Oh-oka H (2004) Function of a PscD subunit in the homodimeric reaction center complex of the photosynthetic green sulfur bacterium Chlorobium tepidum studied by insertional gene inactivation. Regulation of energy transfer and ferredoxin-mediated NADP+ reduction on the cytoplasmic side. J Biol Chem 279: 51122–51130

    PubMed  CAS  Google Scholar 

  • Tsukatani Y, Azai C, Kondo T, Itoh S and Oh-oka H (2008) Parallel electron donation pathways to cytochrome c z in the type I homodimeric photosynthetic reaction center complex of Chlorobium tepidum. Biochim Biophys Acta 1777: 1211–1217

    PubMed  CAS  Google Scholar 

  • Tsukatani Y, Wen J, Blankenship RE and Bryant DA (2010) Characterization of the bacteriochlorophyll a-binding, Fenna-Matthews-Olson protein from Candidatus Chlo­racidobacterium thermophilum. Photosynth Res 104: 201–209

    PubMed  CAS  Google Scholar 

  • Turova TP, Spiridonova EM, Slobodova NV, Bulygina ES, Keppen OI, Kuznetsov BB and Ivanovskiĭ RN (2006) Phylogeny of anoxygenic filamentous phototrophic bacteria of the family Oscillochloridaceae as inferred from comparative analyses of the rrs, cbbL, and nifH genes. Mikrobiologia 75: 235–244

    CAS  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS and Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37–43

    PubMed  CAS  Google Scholar 

  • Vande Weghe JG and Ow DW (1999) A fission yeast gene for mitochondrial sulfide oxidation. J Biol Chem 274: 13250–13257

    PubMed  CAS  Google Scholar 

  • Vassilieva EV, Frigaard N-U and Bryant DA (2000) Chlorosomes: the light-harvesting complexes of the green bacteria. The Spectrum 13: 7–13

    CAS  Google Scholar 

  • Vassilieva EV, Antonkine ML, Zybailov BL, Yang F, Jakobs CU, Golbeck JH and Bryant DA (2001) Electron transfer may occur in the chlorosome envelope: the CsmI and CsmJ proteins of chlorosomes are 2Fe-2S ferredoxins. Biochemistry 40: 564–473

    Google Scholar 

  • Vassilieva EV, Stirewalt VL, Jakobs CU, Frigaard N-U, Inoue-Sakamoto K, Baker MA, Sotak A and Bryant DA (2002) Subcellular localization of chlorosome proteins in Chlorobium tepidum and characterization of three new chlorosome proteins: CsmF, CsmH, and CsmX. Biochemistry 41: 4358–4370

    PubMed  CAS  Google Scholar 

  • Verdecia MA, Larkin RM, Ferrer JL, Riek R, Chory J and Noel JP (2005) Structure of the Mg-chelatase cofactor GUN4 reveals a novel hand-shaped fold for porphyrin binding. PLoS Biol 3:e151

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Vogl K, Wenter R, Dressen M, Schlickenrieder M, Plöscher M, Eichacker L and Overmann J (2008) Identification and analysis of four candidate symbiosis genes from ‘Chlorochromatium aggregatum,’ a highly developed bacterial symbiosis. Environ Microbiol 10: 2842–2856

    PubMed  CAS  Google Scholar 

  • Wada K, Yamaguchi H, Harada J, Niimi K, Osumi S, Saga Y, Oh-oka H, Tamiaki H and Fukuyama K (2006) Crystal structures of BchU, a methyltransferase involved in bacteriochlorophyll c biosynthesis, and its complex with S-adenosylhomocysteine: implications for reaction mechanism. J Mol Biol 360: 839–849

    PubMed  CAS  Google Scholar 

  • Wahlund TM, Woese CR, Castenholz RW and Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156: 81–90

    CAS  Google Scholar 

  • Walter MR, Bauld J and Brock TD (1972) Siliceous algal and bacterial stromatolites in hot spring and geyser effluents of Yellowstone National Park. Science 178: 402–405

    PubMed  CAS  Google Scholar 

  • Wanner G, Vogl K and Overmann J (2008) Ultrastructural characterization of the prokaryotic symbiosis in “Chlorochromatium aggregatum.” J Bacteriol 190: 3721–3730

    PubMed  CAS  Google Scholar 

  • Ward DM (2006) Microbial diversity in natural environments: focusing on fundamental questions. Antonie Van Leeuwenhoek 90: 309–324

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ward DM, Bateson MM, Ferris MJ, Kühl M, Wieland A, Koeppel A and Cohan FM (2006) Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, |structure and function. Phils Trans R Soc Lond B Biol Sci 361: 1997–2008

    Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L and Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75: 2046–2056

    PubMed  CAS  Google Scholar 

  • Watanabe Y, Feick RG and Shiozawa JA (1995) Cloning and sequencing of the genes encoding the light-harvesting B806-866 polypeptides and initial studies on the transcriptional organization of puf2B, puf2A and puf2C in Chloroflexus aurantiacus. Arch Microbiol 63: 124–30

    Google Scholar 

  • Wätzlich D, Bröcker MJ, Uliczka F, Ribbe M, Virus S, Jahn D and Moser J (2009) Chimeric nitrogenase-like enzymes of (bacterio)chlorophyll biosynthesis. J Biol Chem 284: 15530–15540

    PubMed  Google Scholar 

  • Wen J, Zhang H, Gross ML and Blankenship RE (2009) Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. Proc Natl Acad Sci USA 106: 6134–6139

    PubMed  CAS  Google Scholar 

  • Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B and Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362: 834–836

    CAS  Google Scholar 

  • Willows RD (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep 20: 327–341

    PubMed  CAS  Google Scholar 

  • Willows RD and Kriegel AM (2009) Biosynthesis of bacteriochlorophylls in purple bacteria. In: Hunter CN, Daldal F, Thurnauer MC and Beatty JT (eds) Advances in Photosynthesis and Respiration, Vol 28, pp 57–79. Springer, Dordrecht

    Google Scholar 

  • Wu D, Raymond J, Wu M, Chatterji S, Ren Q, Graham JE, Bryant DA, Robb F, Colman A, Tallon LJ, Badger JH, Madupu R, Ward NL and Eisen JA (2009) Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. PLoS One 4: e4207

    PubMed  Google Scholar 

  • Xin Y, Lin S, Montaño GA and Blankenship RE (2005) Purification and characterization of the B808-866 light-harvesting complex from green filamentous bacterium Chloroflexus aurantiacus. Photosynth Res 86: 155–163

    PubMed  CAS  Google Scholar 

  • Xin Y, Lu YK, Fromme R, Fromme P and Blankenship RE (2009) Purification, characterization and crystallization of the menaquinol:fumarate oxidoreductase from the green filamentous photosynthetic bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 1787: 86–96

    PubMed  CAS  Google Scholar 

  • Xiong J (2006) Photosynthesis: what color was its origin? Genome Biol 7: article 245

    Google Scholar 

  • Xiong J and Bauer CE (2002a) Complex evolution of photosynthesis. Annu Rev Plant Biol 53: 503–521

    PubMed  CAS  Google Scholar 

  • Xiong J and Bauer CE (2002b) A cytochrome b origin of photosynthetic reaction centers: an evolutionary link between respiration and photosynthesis. J Mol Biol 322: 1025–1037

    PubMed  CAS  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730

    PubMed  CAS  Google Scholar 

  • Yamada M, Zhang H, Hanada S, Nagashima KV, Shimada K and Matsuura K (2005) Structural and spectroscopic properties of a reaction center complex from the chlorosome-lacking filamentous anoxygenic phototrophic bacterium Roseiflexus castenholzii. J Bacteriol 187: 1702–1709

    PubMed  CAS  Google Scholar 

  • Yanyushin MF, del Rosario MC, Brune DC and Blankenship RE (2005) New class of bacterial membrane oxidoreductases. Biochemistry 44: 10037–10045

    PubMed  CAS  Google Scholar 

  • Yoon K-S, Hille R, Hemann C and Tabita FR (1999) Rubredoxin from the green sulfur bacterium Chlorobium tepidum functions as an electron acceptor for pyruvate ferredoxin oxidoreductase. J Biol Chem 274: 29772–29778

    PubMed  CAS  Google Scholar 

  • Yoon K-S, Bobst C, Hemann CF, Hille R and Tabita FR (2001) Spectroscopic and functional properties of novel 2[4Fe-4S] cluster-containing ferredoxins from the green sulfur bacterium Chlorobium tepidum. J Biol Chem 276: 44027–44036

    PubMed  CAS  Google Scholar 

  • Youvan DC, Bylina EJ, Alberti M, Begusch H and Hearst JE (1984) Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B870 antenna, and flanking polypeptides from R. capsulata. Cell 37: 949–957

    PubMed  CAS  Google Scholar 

  • Yu L, Zhao J, Mühlenhoff U, Chitnis PR, Bryant DA and Golbeck JH 1993) PsaE is required for cyclic electron flow around photosystem I in the cyanobacterium Synechococcus sp. PCC 7002 and Synechocystis sp. PCC 6803. Plant Physiol 103: 171–180

    PubMed  CAS  Google Scholar 

  • Zarzycki J, Schlichting A, Strychalsky N, Müller M, Alber BE and Fuchs G (2008) Mesaconyl-coenzyme A hydratase, a new enzyme of two central carbon metabolic pathways in bacteria. J Bacteriol 290: 1366–1374

    Google Scholar 

  • Zarzycki J, Brecht V, Müller M and Fuchs G (2009) Final steps of an autotrophic pathway: closing the 3-hydroxypropionate bicycle in Chloroflexus aurantiacus. Proc Natl Acad Sci USA 106: 21317–21322

    PubMed  CAS  Google Scholar 

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Acknowledgments

Original research described in this chapter was supported by grants to D. A. B. by the U. S. Department of Energy (DE-FG02-94ER20137), the U. S. National Science Foundation (MCB-0523100), and National Aeronautics and Space Administration: Astrobiology (NNX09AM87G; D. M. W., P. I.). D. A. B. and D. M. W. additionally and gratefully acknowledge support from the U.S. Department of Energy (BER), as part of BER’s Genomic Science Program (GSP). This contribution originates from the GSP Foundational Scientific Focus Area (FSFA) at the Pacific Northwest National Laboratory (PNNL), contract no. 112443. N.-U. F. acknowledges support from the Danish Science Research Council. D. A. B. and J. O. thank the Joint Genome Institute for their assistance in generating draft genomes of some Chlorobiales and completed genomes of Chloroflexales described here. Research of J. O. was supported by grants from the Deutsche Forschungsgemeinschaft (DFG Ov20/8-1 through 8–3, and Ov20/10-1 and 10–2). D. M. W. acknowledges support from NASA (NAG5-8824, 13468 and NX09AM87G), NASA’s support of the Montanta State Thermal Biology Institute (NAG5-8807), and the U. S. National Science Foundation (EF-0328698).

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Bryant, D.A. et al. (2012). Comparative and Functional Genomics of Anoxygenic Green Bacteria from the Taxa Chlorobi, Chloroflexi, and Acidobacteria . In: Burnap, R., Vermaas, W. (eds) Functional Genomics and Evolution of Photosynthetic Systems. Advances in Photosynthesis and Respiration, vol 33. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1533-2_3

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