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Photosynthesis Research

, Volume 97, Issue 2, pp 121–140 | Cite as

The biochemical basis for structural diversity in the carotenoids of chlorophototrophic bacteria

  • Julia A. Maresca
  • Joel E. Graham
  • Donald A. BryantEmail author
Review Paper

Abstract

Ongoing work has led to the identification of most of the biochemical steps in carotenoid biosynthesis in chlorophototrophic bacteria. In carotenogenesis, a relatively small number of modifications leads to a great diversity of carotenoid structures. This review examines the individual steps in the pathway, discusses how each contributes to structural diversity among carotenoids, and summarizes recent progress in elucidating the biosynthetic pathways for carotenoids in chlorophototrophs.

Key words

Carotenoids Carotenogenesis Photosynthesis Lycopene cyclase Cyanobacteria Green sulfur bacteria 

Abbreviations

BChl

Bacteriochlorophyll

Cab.

Chloracidobacterium

Cfx.

Chloroflexus

Chb.

Chlorobaculum

Chl

Chlorophyll

CRTISO

Carotenoid isomerase (plants)

DMAPP

Dimethylallyl pyrophosphate

E.

Escherichia

Erb.

Erythrobacter

FPP

Farnesyl pyrophosphate

GGPP

Geranylgeranyl pyrophosphate

Glb.

Gloeobacter

GSB

Green sulfur bacteria

Hbc.

Heliobacillus

Hbm.

Heliobacterium

Hps.

Herpetosiphon

Htx.

Heliothrix

IPP

Isopentenyl diphosphate

MEP

2C-methyl-D-erythritol 4-phosphate

ORF

Open reading frame

PDS

Phytoene desaturase (plants)

PS

Photosystem

PSB

Purple sulfur bacteria

Rfx.

Roseiflexus

Rhb.

Rhodobacter

Rps.

Rhodopseudomonas

Rsp.

Rhodospirillum

Rvx.

Rubrivivax

S.

Staphylococcus

ZDS

ζ-carotene desaturase (plants)

Notes

Acknowledgements

Research from the laboratory of Donald A. Bryant was generously supported by the US Dept. of Energy (DE-FG02-94ER20137) and National Science Foundation (MCB-0523100 and MCB-0519743).

References

  1. Aakermann T, Skulberg OM, Liaaen-Jensen S (1992) Carotenoids of blue-green algae. 12. A comparison of the carotenoids of the strains of Oscillatoria and Spirulina (cyanobacteria). Biochem Syst Ecol 20:761–769Google Scholar
  2. Albrecht M, Linden H, Sandmann G (1996) Biochemical characterization of purified ζ-carotene desaturase from Anabaena PCC 7120 after expression in Escherichia coli. Eur J Biochem 236:115–120PubMedGoogle Scholar
  3. Albrecht M, Ruther A, Sandmann G (1997) Purification and biochemical characterization of a hydroxyneurosporene desaturase involved in the biosynthetic pathway of the carotenoid spheroidene in Rhodobacter sphaeroides. J Bacteriol 179:7462–7467PubMedGoogle Scholar
  4. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402PubMedGoogle Scholar
  5. Andrews AG, Liaaen-Jensen S (1972) Carotenoids of Thiorhodaceae 9. Structural elucidation of five minor carotenoids from Thiothece gelatinosa. Acta Chem Scand 26:2194–2204Google Scholar
  6. Armstrong GA (1997) Genetics of eubacterial carotenoid biosynthesis: a colorful tale. Annu Rev Microbiol 51:629–659PubMedGoogle Scholar
  7. Armstrong GA, Hearst JE (1996) Genetics and molecular biology of carotenoid biosynthesis. FASEB J 10:228–237PubMedGoogle Scholar
  8. Armstrong GA, Schmidt A, Sanfmann G, Hearst JE (1990) Genetic and biochemical characterization of carotenoid biosynthesis mutants of Rhodobacter capsulatus. J Biol Chem 265:8329–8338PubMedGoogle Scholar
  9. Auldridge ME, McCarty DR, Klee DE (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321PubMedGoogle Scholar
  10. Balashov SP, Imasheva ES, Boichenko VA, Anton J, Wang JM, Lanyi JK (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309:2061–2064PubMedGoogle Scholar
  11. Balashov SP, Imasheva ES, Lanyi JK (2006) Induced chirality of the light-harvesting carotenoid salinixanthin and its interaction with the retinal of xanthorhodopsin. Biochemistry 45:10998–11004PubMedGoogle Scholar
  12. Bartley GE, Scolnik PA, Beyer P (1999) Two Arabidopsis thaliana carotene desaturases, phytoene desaturase and ζ-carotene desaturase, expressed in Escherichia coli, catalyze a poly-cis pathway to yield pro-lycopene. Eur J Biochem 259:396–403PubMedGoogle Scholar
  13. Bautista JA, Rappaport F, Guergova-Kuras M, Cohen RO, Golbeck JG, Wang JY, Beal D, Diner BA (2005) Biochemical and biophysical characterisation of photosystem I from phytoene desaturase and ζ-carotene desaturase deletion mutants of Synechocystis sp. PCC 6803. J Biol Chem 280:20030–20041PubMedGoogle Scholar
  14. Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich S, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906PubMedGoogle Scholar
  15. Bialek-Bylka GE, Fujii R, Chen CH, Oh-oka H, Kamiesu A, Satoh K, Koike H, Koyama Y (1998) 15-cis-carotenoids found in the reaction center of a green sulfur bacterium Chlorobium tepidum and in the Photosystem I reaction center of a cyanobacterium Synechococcus vulcanus. Photosynth Res 58:135–142Google Scholar
  16. Boronowsky U, Wenk SO, Schneider D, Jager C, Rogner M (2001) Isolation of membrane protein subunits in their native state: evidence for selective binding of chlorophyll and carotenoid to the b 6 subunit of the cytochrome b 6 f complex. Biochim Biophys Acta 1506:55–66PubMedGoogle Scholar
  17. Boucher Y, Doolittle WF (2000) The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol Microbiol 37:703–716PubMedGoogle Scholar
  18. Bramley P, Sandmann G (1985) In vitro and in vivo biosynthesis of xanthophylls by the cyanobacterium Aphanocapsa. Phytochemistry 24:2919–2922Google Scholar
  19. Breitenbach J, Sandmann G (2005) ζ-carotene cis-isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta 220:785–793PubMedGoogle Scholar
  20. Breitenbach J, Fernandez-Gonzalez B, Vioque A, Sandmann G (1998) A higher-plant type ζ-carotene desaturase in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 36:725–732PubMedGoogle Scholar
  21. Breitenbach J, Vioque A, Sandmann G (2001) Gene sll0033 from Synechocystis 6803 encodes a carotene isomerase involved in the biosynthesis of all-E lycopene. Z Naturforsch 56:915–17Google Scholar
  22. Britton G, Singh RK, Goodwin TW, Ben-Aziz A (1975) The carotenoids of Rhodomicrobium vannielii (Rhodospirillaceae) and the effect of diphenylamine on the carotenoid composition. Phytochemistry 14:2427–2433Google Scholar
  23. Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoids handbook. Birkhauser, Boston, MAGoogle Scholar
  24. Bryant DA, Frigaard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496PubMedGoogle Scholar
  25. Caumette P, Baulaigue R, Matheron R (1991) Thiocapsa halophila sp. nov., a novel halophilic phototrophic purple sulfur bacterium. Arch Microbiol 155:170–176Google Scholar
  26. Caumette P, Guyoneaud R, Imhoff JF, Suling J, Gorenko V (2004) Thiocapsa marina sp nov., a novel, okenone-containing, purple sulfur bacterium isolated from brackish coastal and marine environments. Int J Syst Evol Microbiol 54:1031–1036PubMedGoogle Scholar
  27. Chamovitz D, Misawa N, Sandmann G, Hirschberg J (1992) Molecular cloning and expression in Escherichia coli of a cyanobacterial gene coding for phytoene synthase, a carotenoid biosynthesis enzyme. FEBS Lett 296:305–310PubMedGoogle Scholar
  28. Cheng Q (2006) Structural diversity and functional novelty of new carotenoid biosynthesis genes. J Ind Microbiol Biotechnol 33:552–559PubMedGoogle Scholar
  29. Cogdell RJ (1988) The functions of pigments in chloroplasts. In: Goodwin TW (ed) Plant pigments. Academic Press, London, pp 222–224Google Scholar
  30. Cunningham FX Jr, Gantt E (2001) One ring or two? Determination of ring number in carotenoids by lycopene epsilon-cyclases. Proc Nat Acad Sci USA 98:2905–2910PubMedGoogle Scholar
  31. Cunningham FX Jr, Sun Z, Chamovitz D, Hirschberg J, Gantt E (1994) Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp. strain PCC7942. Plant Cell 6:1107–1121PubMedGoogle Scholar
  32. Davies BH (1970) A novel sequence for phytoene dehydrogenation in Rhodospirillum rubrum. Biochem J 116:93–99PubMedGoogle Scholar
  33. de la Torre JR, Christianson LM, Béjà O, Suzuki MT, Karl DM, Heidelberg J, DeLong EF (2003) Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc Natl Acad Sci USA 100:12830–12835PubMedGoogle Scholar
  34. Dubey VS, Bhalla R, Luthra R (2003) An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants. J Biosci 28:637–646PubMedGoogle Scholar
  35. Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelon 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, Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514PubMedGoogle Scholar
  36. Eisenreich W, Bacher A, Arigoni D, Rohdich F (2004) Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61:1401–1426PubMedGoogle Scholar
  37. Fernandez-Gonzales B, Sandmann G, Vioque A (1997) A new type of asymmetrically acting β-carotene ketolase is required for the synthesis of echinenone in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 272:9728–9733Google Scholar
  38. Frank HA, Brudvig GW (2004) Redox functions of carotenoids in photosynthesis. Biochemistry 43:8607–8615PubMedGoogle Scholar
  39. Fraser PD, Misawa N, Linden H, Yamano S, Kobayashi K, Sandmann G (1992) Expression in Esherichia coli, purification, and reactivation of the recombinant Erwinia uredovora phytoene desaturase. J Biol Chem 267:19891–19895PubMedGoogle Scholar
  40. Fraser PD, Linden H, Sandmann G (1993) Purification and reactivation of recombinant Synechococcus phytoene desaturase from an overexpressing strain of Escherichia coli. Biochem J 291:687–692PubMedGoogle Scholar
  41. Fraser NJ, Hashimoto H, Cogdell R (2002) Carotenoids and bacterial photosynthesis: the story so far…. Photosynth Res 70:249–256Google Scholar
  42. Frigaard N-U, Maresca JA, Yunker CE, Jones AD, Bryant DA (2004) Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 186:5210–5220PubMedGoogle Scholar
  43. Fromme P, Jordan P, Krauss N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31PubMedGoogle Scholar
  44. Garcia Costas AM, Graham JE, Bryant DA (2008) Ketocarotenoids in chlorosomes of Candidatus Chloracidobacterium thermophilum. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Energy from the sun. Springer, Dordrecht, The Netherlands, pp 1167–1170Google Scholar
  45. Garcia-Asua G, Lang HP, Cogdell RJ, Hunter CN (1998) Carotenoid diversity: a modular role for the phytoene desaturase step. Trends Plant Sci 3:445–449Google Scholar
  46. Garcia-Asua G, Cogdell RJ, Hunter CN (2002) Functional assembly of the foreign carotenoid lycopene into the photosynthetic apparatus of Rhodobacter sphaeroides, achieved by replacement of the native 3-step phytoene desaturase with its 4-step counterpart from Erwinia herbicola. Mol Microbiol 44:233–244PubMedGoogle Scholar
  47. Gich F, Airs RL, Danielsen M, Keely BJ, Abella CA, Garcia-Gil J, Miller M, Borrego CM (2003) Characterization of the chlorosome antenna of the filamentous anoxygenic phototrophic bacterium Chloronema sp. strain UdG9001. Arch Microbiol 180:417–426PubMedGoogle Scholar
  48. Giovannoni SJ, Bibbs L, Cho JC, Stapels MD, Desiderio R, Vergin KL, Rappé MS, Laney S, Wilhelm LJ, Tripp HJ, Mathur EJ, Barofsky DF (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438:82–85PubMedGoogle Scholar
  49. Giraud E, Hannibal L, Fardoux J, Jaubert M, Jourand P, Dreyfus B, Sturgis JN, Vermeglio A (2004) Two distinct crt gene clusters for two different functional classes of carotenoid in Bradyrhizobium. J Biol Chem 279:15076–15083PubMedGoogle Scholar
  50. Giuliano G, Pollock D, Scolnik PA (1986) The gene crtI mediates the conversion of phytoene into colored carotenoids in Rhodopseudomonas capsulata. J Biol Chem 261:12925–12929PubMedGoogle Scholar
  51. Goeriche R, Repeta D (1992) The pigments of Prochlorococcus marinus: the presence of divinyl chlorophyll a and b in a marine prokaryote. Limnol Oceanogr 37:425–433Google Scholar
  52. Gomez Maqueo Chew A, Bryant DA (2007) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu Rev Microbiol 61:113–129Google Scholar
  53. Gómez-Consarnau L, González JM, Coll-Lladó M, Gourdon P, Pascher T, Neutze R, Pedrós-Alió C, Pinhassi J (2007) Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445:210–213PubMedGoogle Scholar
  54. Graham JE (2008) Carotenoid biosynthesis in Synechococcus sp. PCC 7002: identification of genes, enzymes and carotenoids. Ph D thesis, The Pennsylvania State UniversityGoogle Scholar
  55. Graham JE, Lecomte JTJ, Bryant DA (2008) Synechoxanthin: an aromatic C40 xanthophyll is a major carotenoid in the cyanobacterium Synechococcus sp. PCC 7002. J Nat Prod, submitted for publicationGoogle Scholar
  56. Gregonis DE, Rilling HC (1974) The Stereochemistry of trans-phytoene synthesis. Some observations on lycopersene as a carotenoid precursor and a mechanism for the synthesis of trans lycopene. Biochemistry 13:1538–1542PubMedGoogle Scholar
  57. Hanada S, Hiraishi A, Shimada K, Matsuura K (1995) Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement. Int J Syst Bacteriol 45:676–681PubMedCrossRefGoogle Scholar
  58. Hanada S, Takaichi S, Matsuura K, Nakamura K (2002) Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous photosynthetic bacterium that lacks chlorosomes. Int J Syst Evol Microbiol 52:187–193PubMedGoogle Scholar
  59. Harada J, Nagashima KVP, Takaichi S, Misawa N, Matsuura K, Shimada K (2001) Phytoene desaturase, CrtI, of the purple photosynthetic bacterium, Rubrivivax gelatinosus, produces both neurosporene and lycopene. Plant Cell Physiol 42:1112–1118PubMedGoogle Scholar
  60. Hausmann A, Sandmann G (2000) A single five-step desaturase is involved in the carotenoid biosynthesis pathway to beta-carotene and torulene in Neurospora crassa. Fungal Genet Biol 30:147–153PubMedGoogle Scholar
  61. Hemmi H, Ikejiri S, Nakayama T, Nishino T (2003) Fusion-type lycopene β-cyclase from a thermoacidophilic archaeon Sulfolobus solfataricus. Biochem Biophys Res Comm 305:586–591PubMedGoogle Scholar
  62. Hesse K, Dittmann E, Borner T (2001) Consequences of impaired microcystin production for light-dependent growth and pigmentation of Microcystis aeruginosa PCC 7806. FEMS Microbiol Ecol 37:39–43Google Scholar
  63. Hirabiayashi H, Ishii T, Takaichi S, Inoue K, Uehara K (2004) The role of carotenoids in the brown-colored sulfur bacterium Chlorobium phaeobacteroides. Photochem Photobiol 79:280–285Google Scholar
  64. Holt JG, Lewin RA (1968) Herpetosiphon aurantiacus gen. et sp. n., a new filamentous gliding organism. J Bacteriol 95:2407–2408PubMedGoogle Scholar
  65. Hundle BS, O’Brien DA, Alberti M, Meyer P, Hearst JA (1992) Functional expression of a zeaxanthin glucosyltransferase from Erwinia herbicola and a proposed uridine diphosphate binding site. Proc Nat Acad Sci USA 89:9321–9325PubMedGoogle Scholar
  66. Hunter WN (2007) The non-mevalonate pathway of isoprenoid precursor biosynthesis. J Biol Chem 282:21573–21577PubMedGoogle Scholar
  67. Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell 14:333–342PubMedGoogle Scholar
  68. Jordan P, Fromme P, Witt HT, Klukas O, Sanger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–911PubMedGoogle Scholar
  69. Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 308:267–269PubMedGoogle Scholar
  70. Kovács AT, Rákhely G, Kovács KL (2003) Genes involved in the biosynthesis of the photosynthetic pigments in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 69:3093–3102PubMedGoogle Scholar
  71. Krubasik P, Sandmann G (2000a) A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol Gen Genet 263:423–432PubMedGoogle Scholar
  72. Krubasik P, Sandmann G (2000b) Molecular evolution of lycopene cyclases involved in the formation of carotenoids with ionone end groups. Biochem Soc Trans 28:806–810PubMedGoogle Scholar
  73. Krueger BP, Scholes GD, Jimenez R, Fleming GR (1998) Electronic excitation transfer from carotenoid to bacteriochlorophyll in the purple bacterium Rhodopseudomonas acidophila. J Phys Chem B 102:2284–2292Google Scholar
  74. Krugel H, Krubasik P, Weber K, Saluz HP, 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 1439:57–64PubMedGoogle Scholar
  75. Kumar PA, Srinivas TNR, Sasikala C, Ramana CV (2007) Halochromatium roseum sp. nov., a non-motile phototrophic gammaproteobacterium with gas vesicles, and emended description of the genus Halochromatium. Int J Syst Evol Microbiol 57:2110–2113PubMedGoogle Scholar
  76. Kushwaha SC, Kates M (1979) Effect of nicotine on biosynthesis of C50 carotenoids in Halobacterium cutirubrum. Can J Biochem 54:824–829Google Scholar
  77. Kuzuyama T (2002) Mevalonate and nonmevalonate pathways for the biosynthesis of isoprene units. Biosci Biotechnol Biochem 66:1619–1627PubMedGoogle Scholar
  78. Lagarde D, Vermaas WFJ (1999) The zeaxanthin biosynthesis enzyme β-carotene hydroxylase is involved in myxoxanthophyll synthesis in Synechocystis sp. PCC 6803. FEBS Lett 454:247–245PubMedGoogle Scholar
  79. Lakatos M, Bilger W, Budel B (2001) Carotenoid composition of terrestrial Cyanobacteria: response to natural light conditions in open rock habitats in Venezuela. Eur J Phycol 36:367–375Google Scholar
  80. Lang HP, Cogdell RJ, Takaichi S, Hunter CN (1995) Complete DNA sequence, specific Tn5 insertion map, and gene assignment of the carotenoid biosynthesis pathway of Rhodobacter sphaeroides. J Bacteriol 177:2064–2073PubMedGoogle Scholar
  81. Lee PC, Mijts BN, Schmidt-Dannert C (2004) Investigation of factors influencing production of the monocyclic carotenoid torulene in metabolically engineered Escherichia coli. Appl Microbiol Biotechnol 65:538–546PubMedGoogle Scholar
  82. Leutwiler LS, Chapman DJ (1978) Biosynthesis of carotenoids in Rhodomicrobium vannielii. FEBS Lett 89:248–252PubMedGoogle Scholar
  83. Li F, Murillo C, Wurtzel ET (2007) Maize y9 encodes a product essential for 15-cis-ζ-carotene isomerization. Plant Physiol 144:1181–1189PubMedGoogle Scholar
  84. Liaaen-Jensen S (1965) Bacterial carotenoids. XVIII. Aryl carotenoids from Phaeobium. Acta Chemica Scand 19:1025–1030Google Scholar
  85. Liang C, Zhao F, Wei W, Wen Z, Qin S (2006) Carotenoid biosynthesis in cyanobacteria: structural and evolutionary scenarios based on comparative genomics. Int J Biol Sci 2:197–207PubMedGoogle Scholar
  86. Linden H, Misawa N, Chamovitz D, Pecker I, Hirschberg J, Sandmann G (1991) Functional complementation in Escherichia coli of different phytoene desaturase genes and analysis of accumulated carotenes. Z Naturforsch 46:1045–1051Google Scholar
  87. Liu Y, Wang H, Ye H-C, Li G-F (2005) Advances in the plant isoprenoid biosynthesis pathway and its metabolic engineering. J Integ Plant Biol 47:769–782Google Scholar
  88. Liu CI, Liu GY, Song Y, Yin F, Hensler ME, Jeng WY, Nizet V, Wang AH, Oldfield E (2008) A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science 319:1391–1394PubMedGoogle Scholar
  89. Lozier RH, Bogomolni RA, Stoeckenius W (1975) Bacteriorhodopsin: light-driven proton pump in Halobacterium halobium. Biophys J 15:955–962PubMedGoogle Scholar
  90. Macpherson AN, Arellano JB, Fraser NJ, Cogdell RJ, Gillbro T (2001) Efficient energy transfer from the carotenoid S2 state in a photosynthetic light-harvesting complex. Biophys J 80:923–930PubMedGoogle Scholar
  91. Marasco EK, Vay K, Schmidt-Dannert C (2006) Identification of carotenoid cleavage dioxygenases from Nostoc sp. PCC 7120 with different cleavage activities. J Biol Chem 281:31583–31593PubMedGoogle Scholar
  92. Maresca JA (2007) The genetic basis for pigment variation among green sulfur bacteria. Ph D thesis, The Pennsylvania State UniversityGoogle Scholar
  93. Maresca JA, Bryant DA (2006) Two genes encoding new carotenoid-modifying enzymes in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 188:6217–6223PubMedGoogle Scholar
  94. Maresca JA, Graham JE, Wu M, Eisen J, Bryant DA (2007) Identification of a fourth type of carotenoid cyclase in photosynthetic organisms. Proc Natl Acad Sci USA 104:11784–11789PubMedGoogle Scholar
  95. Martinez A, Bradley AS, Waldbauer JR, Summons RE, Delong EF (2007) Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc Nat Acad Sci USA 104:5590–5595PubMedGoogle Scholar
  96. Martinez-Ferez I, Fernandez-Gonzalez B, Sandmann G, Vioque A (1994) Cloning and expression in Escherichia coli the gene coding for phytoene synthase from the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1218:145–152PubMedGoogle Scholar
  97. Masamoto K, Misawa N, Kaneko T, Kikuno R, Toh H (1998) β-carotene hydroxylase gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 39:560–564PubMedGoogle Scholar
  98. Masamoto K, Wada H, Kaneko T, Takaichi S (2001) Identification of a gene required for cis-to-trans carotene isomerization in carotenogenesis of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 42:1398–1402PubMedGoogle Scholar
  99. Math SK, Hearst JE, Poulter CD (1992) The crtE gene in Erwinia herbicola encodes geranylgeranyl diphosphate synthase. Proc Nat Acad Sci USA 89:6761–6764PubMedGoogle Scholar
  100. Matsumura H, Takeyama H, Kusakabe E, Burgess JG, Matsunanga T (1997) Cloning, sequencing, and expressing the carotenoid biosynthesis genes, lycopene cyclase and phytoene desaturase, from the aerobic photosynthetic bacterium Erythrobacter longus sp. strain Och101 in Escherichia coli. Gene 189:169–174PubMedGoogle Scholar
  101. Maudinas B, Herber R, Villoutreix J (1974) Occurrence of tran-phyotene in microorganisms grown in the absence of carotenogenesis inhibitors. Biochim Biophys Acta 348:357–360PubMedGoogle Scholar
  102. McCarren J, DeLong EF (2007) Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ Microbiol 9:846–858PubMedGoogle Scholar
  103. Mijts BN, Lee PC, Schmidt-Dannert C (2004) Engineering carotenoid biosynthetic pathways. Meth Enzymol 388:315–329PubMedGoogle Scholar
  104. Mimuro M, Katoh T (1991) Carotenoids in photosynthesis: absorption, transfer and dissipation of light energy. Pure Appl Chem 63:123–130Google Scholar
  105. Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172:6704–6712PubMedGoogle Scholar
  106. Misawa N, Kajiwara S, Kondo K, Yokoyama A, Satomi Y, Saito T, Miki W, Ohtani T (1995) Canthaxanthin biosynthesis by the conversion of methylene to keto groups in the hydrocarbon β-carotene by a single gene. Biochem Biophys Res Comm 209:867–876PubMedGoogle Scholar
  107. Miskiewicz E, Ivanov AG, Williams JP, Khan MU, Falk S, Huner NPA (2000) Photosynthetic acclimation of the filamentous cyanobacterium, Plectonema boryanum UTEX 485, to temperature and light. Plant Cell Phys 41:767–775Google Scholar
  108. Mochimaru M, Masukawa H, Takaichi S (2005) The cyanobacterium Anabaena sp. PCC 7120 has two distinct β-carotene ketolases: CrtO for echinenone and CrtW for ketomyxol synthesis. FEBS Lett 579:6111–6114PubMedGoogle Scholar
  109. Mohamed HE, Vermaas WFJ (2004) Slr1293 in Synechocystis sp. strain PCC 6803 is the C-3′, 4′ desaturase (CrtD) involved in myxoxanthophyll biosynthesis. J Bacteriol 186:5621–5628PubMedGoogle Scholar
  110. Mohamed HE, Vermaas WFJ (2006) Sll0254 (CrtL(diox)) is a bifunctional lycopene cyclase/dioxygenase in cyanobacteria producing myxoxanthophyll. J Bacteriol 188:3337–3344PubMedGoogle Scholar
  111. Moskalenko AA, Makhevna ZK, Fiedor L, Scheer H (2005) Effects of carotenoid inhibition on the photosynthetic RC-LHI complex in purple sulphur bacterium Thiorhodospira sibirica. Photosynth Res 86:71–80PubMedGoogle Scholar
  112. Nagae H, Kakitani T, Katoh T, Mimuro M (1993) Calculation of the excitation transfer-matrix elements between the S(2) or S(1) state of carotenoid and the S(2) or S(1) state of bacteriochlorophyll. J Chem Phys 98:8012–8023Google Scholar
  113. Neudert U, Martinez-Ferez IM, Fraser PD, Sandmann G (1998) Expression of an active phytoene synthase from Erwinia uredovora and biochemical properties of the enzyme. Biochim Biophys Acta 1392:51–58PubMedGoogle Scholar
  114. Nishida Y, Adachi K, Kasai H, Shizuri Y, Shindo K, Sawabe A, Komemushi S, Miki W, Misawa N (2005) Elucidation of a carotenoid biosynthesis gene cluster encoding a novel enzyme, 2, 2′-beta-hydroxylase, from Brevundimonas sp. strain SD212 and a combinatorial biosynthesis of new or rare xanthophylls. Appl Environ Microbiol 71:4286–4296PubMedGoogle Scholar
  115. Okada K, Minehira M, Zhu X, Suzuki K, Nakagawa T, Matsuda H, Kawamukai M (1997) The ispB gene encoding octaprenyl diphosphate synthase is essential for growth of Escherichia coli. J Bacteriol 179:3058–3060PubMedGoogle Scholar
  116. Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332PubMedGoogle Scholar
  117. Peck RF, Echevarri-Erasun C, Johnson EA, Ng WV, Kennedy SP, Hood L, DasSarma S, Krebs MP (2001) brp and blh are required for synthesis of the retinal cofactor of bacteriorhodopsin in Halobacterium salinarum. J Biol Chem 276:5739–5744PubMedGoogle Scholar
  118. Peck RF, Johnson EA, Krebs MP (2002) Identification of a lycopene beta-cyclase required for bacteriorhodopsin biogenesis in the archaeon Halobacterium salinarum. J Bacteriol 184:2889–2897PubMedGoogle Scholar
  119. Pfander H (1994) C45- and C50-carotenoids. Pure Appl Chem 66:2369–2374Google Scholar
  120. Pierson BK, Giovannoni SJ, Stahl DA, Castenholz RW (1985) Heliothrix oregonensis, gen. nov., sp. nov., a phototrophic filamentous gliding bacterium containing bacteriochlorophyll a. Arch Microbiol 142:164–167PubMedGoogle Scholar
  121. Pinta V, Ouchane S, Picaud M, Takaichi S, Astier C, Reiss-Husson F (2003) Characterization of unusual hydroxy- and ketocarotenoids in Rubrivivax gelatinosus: involvement of enzyme CrtF or CrtA. Arch Microbiol 179:354–362PubMedGoogle Scholar
  122. Psencik J, Ma YZ, Arellano JB, Garcia-Gil J, Holzwarth AR, Gillbro T (2002) Excitation energy transfer in chlorosomes of Chlorobium phaeobacteroides strain CL1401: the role of carotenoids. Photosynth Res 71:5–18PubMedGoogle Scholar
  123. Qureshi N, Porter JW (1981) Conversion of acetyl-coenzyme A to isopentenyl pyrophosphate. In: Porter JW, Spurgeon SL (eds) Biosynthesis of isoprenoid compounds vol 1. Wiley, New York, pp 47–94Google Scholar
  124. Raisig A, Sandmann G (2001) Functional properties of diapophytoene and related desaturases of C30 and C40 carotenoid biosynthetic pathways. Biochim Biophys Acta 1533:164–170PubMedGoogle Scholar
  125. Raisig A, Bartley G, Scolnik P, Sandmann G (1996) Purification in an active state and properties of the 3-step phytoene desaturase from Rhodobacter capsulatus overexpressed in Escherichia coli. J Biochem 119:559–564PubMedGoogle Scholar
  126. Rieder C, Strauss G, Fuchs G, Arigoni D, Bacher A, Eisenreich W (1998) Biosynthesis of the diterpene verrucosan-2β-ol in the phototrophic eubacterium Chloroflexus aurantiacus. J Biol Chem 273:18099–18108PubMedGoogle Scholar
  127. Ritz T, Damjanovic A, Schulten K, Zhang J-P, Koyama Y (2000) Efficient light harvesting through carotenoids. Photosynth Res 66:125–144PubMedGoogle Scholar
  128. Rohdich F, Bacher A, Eisenreich W (2004) Perspectives in anti-infective drug design: the late steps in the biosynthesis of the universal terpenoid precursors, isopentenyl diphosphate and dimethylallyl diphosphate. Bioorg Chem 32:292–308PubMedGoogle Scholar
  129. Ruch S, Beyer P, Ernst H, Al-Babili S (2005) Retinal biosynthesis in eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol Microbiol 55:1015–1024PubMedGoogle Scholar
  130. Sabehi G, Loy A, Jung K-H, Partha R, Spudich JL, Isaacson T, Hirschberg J, Wagner M, Béjà O (2005) New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol 3:1409–1417Google Scholar
  131. Sandmann G (1991) Light-dependent switch from formation of poly-cis carotenes to all-trans carotenoids in the Scenedesmus mutant C-6D. Arch Microbiol 155:229–233Google Scholar
  132. Sandmann G, Misawa N (1992) New functional assignment of the carotenogenic genes crtB and crtE with constructs of these genes from Erwinia species. FEMS Microbiol Lett 90:253–258Google Scholar
  133. Santoyo S, Herrero M, Senorans FJ, Cifuentes A, Ibanez E, Jaime L (2006) Functional characterization of pressurized liquid extracts of Spirulina platensis. Eur Food Res Technol 224:75–81Google Scholar
  134. Schafer L, Vioque A, Sandmann G (2005) Functional in situ evaluation of photosynthesis-protecting carotenoids in mutants of the cyanobacterium Synechocystis sp. PCC 6803. J Photochem Photobiol B 78:195–201PubMedGoogle Scholar
  135. Schagerl M, Donabaum K (2003) Patterns of major photosynthetic pigments in freshwater algae. 1. Cyanoprokaryota, Rhodophyta, and Cryptophyta. Int J Limnol 39:35–47Google Scholar
  136. Schagerl M, Muller B (2006) Acclimation of chlorophyll a and carotenoid levels to different irradiances in four freshwater cyanobacteria. J Plant Phys 163:709–716Google Scholar
  137. Scherzinger D, Ruch S, Kloer DP, Wilde A, Al-Babili S (2006) Retinal is formed from apo-carotenoids in Nostoc sp. 7120: in vitro characterization of an apo-carotenoid oxygenase. Biochem J 398:361–369PubMedGoogle Scholar
  138. Schluter L, Garde K, Kaas H (2004) Detection of the toxic cyanobacteria Nodularia spumigena by means of a 4-keto-myxoxanthophyll-like pigment in the Baltic Sea. Marine Ecol Prog Series 275:69–78Google Scholar
  139. Schmidt K (1980) A comparative study on the composition of chlorosomes (Chlorobium vesicles) and cytoplasmic membranes from Chloroflexus aurantiacus strain Ok-70-fl and Chlorobium limicola f. thiosulfatophilum strain 6230. Arch Microbiol 124:21–31Google Scholar
  140. Schmidt K, Liaaen-Jensen S (1973) Bacterial carotenoids. XLII. New keto-carotenoids from Rhodopseudomonas globiformis (Rhodospirillaceae). Acta Chem Scand 27:3040–3052PubMedCrossRefGoogle Scholar
  141. Schneider C, Boger P, Sandmann G (1997) Phytoene desaturase: heterologous expression in an active state, purification, and biochemical properties. Protein Expres Purif 10:175–179Google Scholar
  142. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DA (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874PubMedGoogle Scholar
  143. Scolnik PA, Walker MA, Marrs BL (1980) Biosynthesis of carotenoids derived from neurosporene in Rhodopseudomonas capsulata. J Biol Chem 255:2427–2432PubMedGoogle Scholar
  144. Sidorova TN, Makhneva ZK, Puchkova NN, Gorlenko VM, Erokhin YE, Moskalenko AA (1998) Characteristics of the photosynthetic apparatus of the purple bacterium Thiocapsa sp. BM3 containing okenone as a major carotenoid. Microbiology 67:158–164Google Scholar
  145. Spudich JL (2006) The multitalented microbial sensory rhodopsins. Trends Microbiol 14:480–487PubMedGoogle Scholar
  146. Spudich JL, Yang C-S, Jung K-H, Spudich EN (2000) Retinylidene proteins: structures and functions from archaea to humans. Annu Rev Cell Dev Biol 16:365–392PubMedGoogle Scholar
  147. Steiger S, Sandmann G (2004) Cloning of two carotenoid ketolase genes from Nostoc punctiforme for the heterologous production of canthaxanthin and astaxanthin. Biotechnol Lett 26:813–817PubMedGoogle Scholar
  148. Steiger S, Astier A, Sandmann G (2000) Substrate specificity of the expressed carotenoid 3, 4 desaturase from Rubrivivax gelatinosus reveals the detailed reaction sequence to spheroidene and spirilloxanthin. Biochem J 349:635–640PubMedGoogle Scholar
  149. Steiger S, Takaichi S, Sandmann G (2002) Heterologous production of two unusual acyclic carotenoids, 1, 1′-dihydroxy-3, 4-didehydrolycopene and 1-hydroxy-3, 4, 3′, 4′-tetradehydrolycopene by combination of the crtC and crtD genes from Rhodobacter and Rubrivivax. J Biotechnol 97:51–58PubMedGoogle Scholar
  150. Steiger S, Jackisch Y, Sandmann G (2005) Carotenoid biosynthesis in Gloeobacter violaceus PCC4721 [sic] involves a single crtI-type phytoene desaturase instead of typical cyanobacterial enzyme. Arch Microbiol 184:207–214PubMedGoogle Scholar
  151. Stickforth P, Sandmann G (2007) Kinetic variations determine the product pattern of phytoene desaturase from Rubrivivax gelatinosus. Arch Biochem Biophys 461:235–241PubMedGoogle Scholar
  152. Stickforth P, Steiger S, Hess WR, Sandmann G (2003) A novel type of lycopene epsilon-cyclase in the marine cyanobacterium Prochlorococcus marinus MED4. Arch Microbiol 179:409–415PubMedGoogle Scholar
  153. Sumii M, Furutani Y, Waschuk SA, Brown LS, Kandori H (2005) Strongly hydrogen-bonded water molecule present near the retinal chromophore of Leptosphaeria rhodopsin, the bacteriorhodopsin-like proton pump from a eukaryote. Biochemistry 44:15159–15166PubMedGoogle Scholar
  154. Takaichi S (1999) Carotenoids and carotenogenesis in anoxygenic photosynthetic bacteria. In: Frank HA, Young AJ, Britton G, Cogdell R (eds) Advances in photosynthesis and respiration, vol 8, The photochemistry of carotenoids. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 39–69Google Scholar
  155. Takaichi S, Shimada K (1999) Pigment composition of two pigment-protein complexes derived from anaerobically and aerobically grown Rubrivivax gelatinosus and identification of a new ketocarotenoid, 2-ketospirilloxanthin. Plant Cell Phys 40:613–617Google Scholar
  156. Takaichi S, Shimada K, Ishidu J-I (1990) Carotenoids from the aerobic photosynthetic bacterium, Erythrobacter longus: β-carotene and its hydroxyl derivatives. Arch Microbiol 153:118–122Google Scholar
  157. Takaichi S, Inoue K, Akaike M, Kobayashi M, Oh-Oka H, Madigan MT (1997a) The major carotenoid in all known species of heliobacteria is the C30 carotenoid 4, 4′ diaponeurosporene, not neurosporene. Arch Microbiol 168:277–281PubMedGoogle Scholar
  158. Takaichi S, Wang Z-W, Umetsu M, Nozawa T, Shimada K, Madigan MT (1997b) New carotenoids from the thermophilic green sulfur bacterium Chlorobium tepidum: 1′, 2′-dihydro-γ-carotene, 1′, 2′-dihydrochlorobactene, and OH-chlorobactene glucoside ester, and the carotenoid composition of different strains. Arch Microbiol 168:270–276PubMedGoogle Scholar
  159. Takaichi S, Maoka T, Yamada M, Matsuura K, Haikawa Y, Hanada S (2001) Absence of carotenes and presence of a tertiary methoxy group in a carotenoid from a thermophilic filamentous photosynthetic bacterium Roseiflexus castenholzii. Plant Cell Physiol 42:1355–1362PubMedGoogle Scholar
  160. Takaichi S, Mochimaru M, Maoka T, Katoh H (2005) Myxol and 4-ketomyxol 2′-fucosides, not rhamnosides, from Anabaena sp. PCC 7120 and Nostoc punctiforme sp. PCC 73102, and proposal for the biosynthetic pathway of carotenoids. Plant Cell Physiol 46:497–504PubMedGoogle Scholar
  161. Takaichi S, Mochimaru M, Maoka T (2006) Presence of free myxol and 4-hydroxymyxol and absence of myxol glycosides in Anabaena variabilis ATCC 29413, and proposal of a biosynthetic pathway of carotenoids. Plant Cell Physiol 47:211–216PubMedGoogle Scholar
  162. Tao L, Cheng Q (2004) Novel β-carotene ketolases from non-photosynthetic bacteria for canthaxanthin biosynthesis. Mol Gen Genomics 272:530–537Google Scholar
  163. Tao L, Picataggio S, Rouviere PE, Cheng Q (2004) Asymmetrically acting lycopene beta-cyclases (CrtLm) from non-photosynthetic bacteria. Mol Genet Genomics 271:180–188PubMedGoogle Scholar
  164. Tao L, Schenzle A, Odom JM, Cheng Q (2005) Novel carotenoid oxidase involved in biosynthesis of 4, 4′-diapolycopene dialdehyde. Appl Environ Microbiol 71:3294–3301PubMedGoogle Scholar
  165. Tao L, Rouviere PE, Cheng Q (2006) A carotenoid synthesis gene cluster from a non-marine Brevundimonas that synthesizes hydroxylated astaxanthin. Gene 379:101–108PubMedGoogle Scholar
  166. Teramoto M, Takaichi S, Inomata Y, Ikenaga H, Misawa N (2003) Structural and functional analysis of a lycopene beta-monocyclase gene isolated from a unique marine bacterium that produces myxol. FEBS Lett 545:120–126PubMedGoogle Scholar
  167. Thornburg LD, Lai MT, Wishnok JS, Stubbe J (1993) A non-heme iron protein with heme tendencies: an investigation of the substrate specificity of thymine hydroxylase. Biochemistry 32:14023–14033PubMedGoogle Scholar
  168. Tsuchiya T, Takaichi S, Misawa N, Maoka T, Miyashita H, Mimuro M (2005) The cyanobacterium Gloeobacter violaceus PCC 7421 uses bacterial-type phytoene desaturase in carotenoid biosynthesis. FEBS Lett 579:2125–2129PubMedGoogle Scholar
  169. Varkonyi Z, Masamoto K, Debreczeny M, Zsiros O, Ughy B, Gombos Z, Domonkos I, Farkas T, Wada H, Szalontai B (2002) Low-temperature-induced accumulation of xanthophylls and its structural consequences in the photosynthetic membranes of the cyanobacterium Cylindrospermopsis raciborskii: an FTIR spectroscopic study. Proc Natl Acad Sci USA 99:2410–2415PubMedGoogle Scholar
  170. Viveiros M, Krubasik P, Sandmann G, Houssaini-Iraqui M (2000) Structural and functional analysis of the gene cluster encoding carotenoid biosynthesis in Mycobacterium aurum A+. FEMS Microbiol Lett 187:95–101PubMedGoogle Scholar
  171. Vogl K, Glaeser J, Pfannes KR, Wanner G, Overmann R (2006) Chlorobium chlorochromatii sp nov., a symbiotic green sulfur bacterium isolated from the phototrophic consortium “Chlorochromatium aggregatum”. Arch Microbiol 185:363–372PubMedGoogle Scholar
  172. Wehling A, Walla PJ (2005) Time-resolved two-photon spectroscopy of photosystem I determines hidden carotenoid dark-state dynamics. J Phys Chem B 109:24510–24516PubMedGoogle Scholar
  173. Wenk SO, Schneider D, Boronowsky U, Jager C, Klughammer C, de Weerd FL, van Roon H, Vermaas WFJ, Dekker JP, Rogner M (2005) Functional implications of pigments bound to a cyanobacterial cytochrome b 6 f complex. FEBS J 272:582–592PubMedGoogle Scholar
  174. Wieland B, Feil C, Gloria-Maercker E, Thumm G, Lechner M, Bravo J-M, Poralla K, Gotz F (1994) Genetic and biochemical analyses of the biosynthesis of the yellow carotenoid 4, 4′-diaponeurosporene of Staphylococcus aureus. J Bacteriol 176:7719–7726PubMedGoogle Scholar
  175. Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95:14851–14856PubMedGoogle Scholar
  176. Ye RW, Stead KJ, Yao H, He H (2006) Mutational and functional analysis of the β-carotene ketolase involved in the production of canthaxanthin and astaxanthin. Appl Environ Microbiol 72:5829–5837PubMedGoogle Scholar
  177. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystral structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Julia A. Maresca
    • 1
    • 2
  • Joel E. Graham
    • 1
  • Donald A. Bryant
    • 1
    Email author
  1. 1.Department of Biochemistry and Molecular BiologyThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Civil and Environmental Engineering, Division of Biological EngineeringMassachusetts Institute of TechnologyCambridgeUSA

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