Carbon metabolic pathways in phototrophic bacteria and their broader evolutionary implications

Frontiers in Microbiology

Volumn 2, Issue AUG, 2011, Pages

  Tang, Kuo Hsiang ^a,c   Tang, Yinjie J ^b   Blankenship, Robert Eugene ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^c CLARK UNIVERSITY   (United States)

Author keywords

Acetate assimilation; Biomass and biofuel; Citrate metabolism; Metabolomics; Photosynthesis; Unconventional pathways and enzymes

Indexed keywords

PHOTOBACTERIA;

EID: 83755218329     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00165     Document Type: Review

References (181)

1. Ahmed, H., Ettema, T. J., Tjaden, B., Geerling, A. C., van der Oost, J., and Siebers, B. (2005). The semi-phosphorylative Entner-Doudoroff pathway in hyperther-mophilic archaea: a re-evaluation. Biochem. J. 390, 529-540.
2. Alber, B. E., Spanheimer, R., Ebenau-Jehle,C.,and Fuchs,G. (2006). Study of an alternate glyoxylate cycle for acetate assimilation by Rhodobac-ter sphaeroides. Mol. Microbiol. 61, 297-309.
3. Albers, H., and Gottschalk, G. (1976). Acetate metabolism in Rhodopseudomonas gelatinosa and several other Rhodospirillaceae. Arch. Microbiol. 111, 45-49.
4. Allard, J., Grochulski, P., and Sygusch, J. (2001). Covalent intermediate trapped in 2-keto-3-deoxy-6-phos-phogluconate (KDPG) aldolase structure at 1.95-A resolution. Proc. Natl. Acad. Sci. U.S.A. 98, 3679-3684.
5. Aoshima, M., Ishii, M., and Igarashi, Y. (2004a). A novel enzyme, citryl-CoA synthetase, catalysing the first step of the citrate cleavage reaction in Hydrogenobacter thermophilus TK-6. Mol. Microbiol. 52, 751-761.
6. Aoshima, M., Ishii, M., and Igarashi, Y. (2004b). A novel enzyme, citryl-CoA lyase, catalysing the second step of the citrate cleavage reaction in Hydrogenobacter thermophilus TK-6. Mol. Microbiol. 52, 763-770.
7. Astier, C., Elmorjani, K., Meyer, I., Joset, F., and Herdman, M. (1984). Photo-synthetic mutants of the cyanobac-teria Synechocystis sp. strains PCC 6714 and PCC 6803: sodium p-hydroxymercuribenzoate as a selec-tive agent. J. Bacteriol. 158, 659-664
8. Bandyopadhyay, A., Stockel, J., Min, H., Sherman, L. A., and Pakrasi, H. B. (2010). High rates of photobiolog-ical H2 production by a cyanobac-terium under aerobic conditions. Nat. Commun. 1, 139.
9. Bassham, J. A., Benson, A. A., and Calvin, M. (1950). The path of car-bon in photosynthesis. J. Biol. Chem. 185, 781-787.
10. Berg, I. A., Keppen, O. I., Krasilnikova, E. N., Ugolkova, N. V., and Ivanovskii, R. N. (2005). Carbon metabolism of filamentous anoxy-genic phototrophic bacteria of the family Oscillochloridaceae. Microbi-ology 74, 258-264.
11. Berg, I. A., Kockelkorn, D., Buckel, W., and Fuchs, G. (2007). A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation path-way in archaea. Science 318, 1782-1786.
12. Berg, I. A., Kockelkorn, D., Ramos-Vera, W. H., Say, R. F., Zarzycki, J., Hugler, M., Alber, B. E., and Fuchs, G. (2010). Autotrophic carbon fixa-tion in archaea. Nat. Rev. Microbiol. 8, 447-460.
13. Bergman,B.,Gallon,J. R.,Rai,A. N.,and Sta, L. J. (1997). N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol. Rev. 19, 139-185.
14. Biebl, H., Allgaier, M., Tindall, B. J., Koblizek, M., Lunsdorf, H., Pukall, R., and Wagner-Dobler, I. (2005). Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagel-lates. Int. J. Syst. Evol. Microbiol. 55, 1089-1096.
15. Biebl, H., Tindall, B. J., Pukall, R., Luns-dorf, H., Allgaier, M., and Wagner-Dobler, I. (2006). Hoeflea pho-totrophica sp. nov., a novel marine aerobic alphaproteobacterium that forms bacteriochlorophyll a. Int. J. Syst. Evol. Microbiol. 56, 821-826.
16. Blankenship, R. E. (2002). Molecu-lar Mechanisms of Photosynthesis. Oxford: Blackwell Science Ltd.
17. Bricker, T. M., Zhang, S., Laborde, S. M., Mayer, P. R. III, Frankel, L. K., and Moroney, J. V. (2004). The malic enzyme is required for optimal pho-toautotrophic growth of Synechocys-tis sp. strain PCC 6803 under con-tinuous light but not under a diur-nal light regimen. J. Bacteriol. 186, 8144-8148.
18. Brinkhoff, T., Giebel, H. A., and Simon, M. (2008). Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch. Microbiol. 189, 531-539.
19. Bryant, D. A., Costas, A. M., Maresca, J. A., Chew,A. G., Klatt, C. G., Bateson, M. M., Tallon, L. J., Hostetler, J., Nelson, W. C., Heidelberg, J. F., and Ward, D. M. (2007). Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Aci-dobacterium. Science 317, 523-526.
20. Bryant, D. A., and Frigaard, N. U. (2006). Prokaryotic photosynthe-sis and phototrophy illuminated. Trends Microbiol. 14, 488-496.
21. Bryantseva, I. A., Gorlenko,V. M., Kom-pantseva, E. I., Achenbach, L. A., and Madigan, M. T. (1999). Heliorestis daurensis, gen. nov. sp.nov., an alka-liphilic rod-to-coiled-shaped pho-totrophic heliobacterium from a siberian soda lake. Arch Microbiol 172, 167-174.
22. Buchanan, B. B., and Arnon, D. I. (1990). A reverse KREBS cycle in photosynthesis: consensus at last. Photosyn. Res. 24, 47-53.
23. Calvin, M. (1989). 40 years of photo-synthesis and related activities. Pho-tosyn. Res. 21, 3-16.
24. Calvin, M., and Benson, A. A. (1948). The path of carbon in photosynthe-sis. Science 107, 476-480.
25. Carr, N. G. (1973). Mechanism of autotrophic physiology in blue green algae. J. Gen. Microbiol. 75, R5-R6.
26. Chen, Y. B., Dominic, B., Mellon, M. T., and Zehr, J. P. (1998). Circa-dian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. strain IMS 101. J. Bacteriol. 180, 3598-3605.
27. Cheriyan, M., Toone, E. J., and Fierke, C. A. (2007). Mutagenesis of the phosphate-binding pocket of KDPG aldolase enhances selectivity for hydrophobic substrates. Protein Sci. 16, 2368-2377.
28. Chu, K. Y., Lin, Y., Hendel, A., Kulpa, J. E., Brownsey, R. W., and Johnson, J. D. (2010). ATP-citrate lyase reduction mediates palmitate-induced apoptosis in pancreatic beta cells. J. Biol. Chem. 285, 32606-32615.
29. Conrad, R., and Schlegel, H. G. (1977). Different degradation path-ways for glucose and fructose in Rhodopseudomonas capsulata. Arch. Microbiol. 112, 39-48.
30. Conrad, R., and Schlegel, H. G. (1978). An alternative pathway for the degradation of endogenous fructose during the catabolism of sucrose in Rhodopseudomonas capsulata. J. Gen. Microbiol. 105, 305-313.
31. Conway, T. (1992). The Entner-Doudoroff pathway: history, physi-ology and molecular biology. FEMS Microbiol. Rev. 9, 1-27.
32. Cossar, J. D., Rowell, P., and Stewart, W. D. P. (1984). Thioredoxin as a mod-ulator of glucose-6-phosphate dehy-drogenase in a N2-fixing cyanobac-terium. J. Gen. Microbiol. 130, 991-998.
33. Davenport, C., Ussery, D. W., and Tummler, B. (2010). Comparative genomics of green sulfur bacteria. Photosyn. Res. 104, 137-152.
34. de Vrije, T., Mars, A. E., Budde, M. A., Lai, M. H., Dijkema, C., de Waard, P., and Claassen, P. A. (2007). Glycolytic pathway and hydrogen yield studies of the extreme ther-mophile Caldicellulosiruptor saccha-rolyticus. Appl. Microbiol. Biotechnol. 74, 1358-1367.
35. Dobrinski, K. P., Longo, D. L., and Scott, K. M. (2005). The carbon-concentrating mechanism of the hydrothermal vent chemolithoau-totroph Thiomicrospira crunogena. J. Bacteriol. 187, 5761-5766.
36. Doolittle, W. F. (1998). You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307-311.
37. Eisen, J. A., Nelson, K. E., Paulsen, I. T., Heidelberg, J. F., Wu, M., Dod-son, R. J., Deboy, R., Gwinn, M. L., Nelson, W. C., Haft, D. H., Hickey, E. K., Peterson, J. D., Durkin, A. S., Kolonay, J. L., Yang, F., Holt, I., Umayam, L. A., Mason, T., Brenner, M., Shea, T. P., Parksey, D., Nierman, W. C., Feldblyum, T. V., Hansen, C. L., Craven, M. B., Radune, D., Vamathevan, J., Khouri, H., White, O., Gruber, T. M., Ketchum, K. A., Venter, J. C., Tettelin, H., Bryant, D. A., and Fraser, C. M. (2002). The complete genome sequence of Chlorobium tepidum TLS, a pho-tosynthetic, anaerobic, green-sulfur bacterium. Proc. Natl. Acad. Sci. U.S.A. 99, 9509-9514.
38. Ensign, S. A. (2006). Revisiting the gly-oxylate cycle: alternate pathways for microbial acetate assimilation. Mol. Microbiol. 61, 274-276.
39. Erb, T. J., Berg, I. A., Brecht, V., Muller, M., Fuchs, G., and Alber, B. E. (2007). Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxy-lase/reductase: the ethylmalonyl-CoA pathway. Proc. Natl. Acad. Sci. U.S.A. 104, 10631-10636.
40. Erb, T. J., Fuchs, G., and Alber, B. E. (2009). (2S)-Methylsuccinyl-CoA dehydrogenase closes the ethylmalonyl-CoA pathway for acetyl-CoA assimilation. Mol. Microbiol. 73, 992-1008.
41. Evans, M. C., Buchanan, B. B., and Arnon, D. I. (1966a). New cyclic process for carbon assimilation by a photosynthetic bacterium. Science 152, 673.
42. Evans, M. C., Buchanan, B. B., and Arnon, D. I. (1966b). A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc. Natl. Acad. Sci. U.S.A. 55, 928-934.
43. Falcone, D. L., and Tabita, F. R. (1991). Expression of endogenous and foreign ribulose 1,5-bisphosphate carboxylase-oxygenase (RubisCO) genes in a RubisCO deletion mutant of Rhodobacter sphaeroides. J. Bacte-riol. 173, 2099-2108.
44. Feng, X., Bandyopadhyay, A., Berla, B., Page, L., Wu, B., Pakrasi, H. B., and Tang, Y. J. (2010a). Mixotrophic and photoheterotrophic metabolism in Cyanothece sp. ATCC 51142 under continuous light. Microbiology 156, 2566-2574.
45. Feng, X., Tang, K. H., Blankenship, R. E., and Tang, Y. J. (2010b). Meta-bolic flux analysis of the mixotrophic metabolisms in the green sulfur bac-terium Chlorobaculum tepidum. J. Biol. Chem. 285, 39544-39550.
46. Feng, X., Mouttaki, H., Lin, L., Huang, R., Wu, B., Hemme, C. L., He, Z., Zhang, B., Hicks, L. M., Xu, J., Zhou, J., and Tang, Y. J. (2009). Char-acterization of the central meta-bolic pathways in Thermoanaerobac-ter sp. X514 via isotopomer-assisted metabolite analysis. Appl. Environ. Microbiol. 75, 5001-5008.
47. Franke, D., Hsu, C. C., and Wong, C. H. (2004). Directed evolution of aldolases. Meth. Enzymol. 388, 224-238.
48. Fuchs, B. M., Spring, S., Teeling, H., Quast, C., Wulf, J., Schattenhofer, M., Yan, S., Ferriera, S., Johnson, J., Glockner, F. O., and Amann, R. (2007). Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 2891-2896.
49. Fuhrer, T., Fischer, E., and Sauer, U. (2005). Experimental identification and quantification of glucose metab-olism in seven bacterial species. J. Bacteriol. 187, 1581-1590.
50. Fullerton, S. W., Griffiths, J. S., Merkel, A. B., Cheriyan, M., Wymer, N. J., Hutchins, M. J., Fierke, C. A., Toone, E. J., and Naismith, J. H. (2006). Mechanism of the class I KDPG aldolase. Bioorg. Med. Chem. 14, 3002-3010.
51. Furch, T., Preusse, M., Tomasch, J., Zech, H., Wagner-Dobler, I., Rabus, R., and Wittmann, C. (2009). Meta-bolic fluxes in the central car-bon metabolism of Dinoroseobac-ter shibae and Phaeobacter gallae-ciensis, two members of the marine Roseobacter clade. BMC Microbiol. 9, 209. doi: 10.1186/1471-2180-9-209
52. Galperin, M. Y., Bairoch, A., and Koonin, E. V. (1998). A super-family of metalloenzymes unifies phosphopentomutase and cofactor-independent phosphoglycerate mutase with alkaline phosphatases and sulfatases. Protein Sci. 7, 1829-1835.
53. Griffiths, J. S., Wymer, N. J., Njolito, E., Niranjanakumari, S., Fierke, C. A., and Toone, E. J. (2002). Cloning, isolation and characterization of the Thermotoga maritima KDPG aldolase. Bioorg. Med. Chem. 10, 545-550.
54. Grochowski, L. L., and White, R. H. (2008). Promiscuous anaerobes: new and unconventional metabo-lism in methanogenic archaea. Ann. N. Y. Acad. Sci. 1125, 190-214.
55. Hagen, K. D., and Meeks, J. C. (2001). The unique cyanobacterial protein OpcA is an allosteric effector of glucose-6-phosphate dehydrogenase in Nostoc punctiforme ATCC 29133. J. Biol. Chem. 276, 11477-11486.
56. Hallenbeck, P. L., Lerchen, R., Hessler, P., and Kaplan, S. (1990a). Roles of CfxA, CfxB, and external elec-tron acceptors in regulation of ribulose 1,5-bisphosphate car-boxylase/oxygenase expression in Rhodobacter sphaeroides. J. Bacteriol. 172, 1736-1748.
57. Hallenbeck, P. L., Lerchen, R., Hessler, P., and Kaplan, S. (1990b). Phos-phoribulokinase activity and regu-lation of CO2 fixation critical for photosynthetic growth of Rhodobac-ter sphaeroides. J. Bacteriol. 172, 1749-1761.
58. Hanada, S., and Pierson, B. K. (2006). The Family Chloroflexaceae. The Prokaryotes, 3rd Edn, Vol. 7. New York: Springer, 815-842.
59. Hanada, S., Takaichi, S., Matsuura, K., and Nakamura, K. (2002). Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bac-terium that lacks chlorosomes. Int. J. Syst. Evol. Microbiol. 52, 187-193.
60. Heinnickel, M., and Golbeck, J. H. (2007). Heliobacterial photosynthe-sis. Photosyn. Res. 92, 35-53.
61. Herter, S., Fuchs, G., Bacher, A., and Eisenreich, W. (2002). A bicyclic autotrophic CO2 fixation pathway in Chloroflexus aurantiacus. J. Biol. Chem. 277, 20277-20283.
62. Hohmann-Marriott, M. F., and Blankenship, R. E. (2011). Evolution of photosynthesis. Annu. Rev. Plant Biol. 62, 515-548.
63. Holo, H. (1989). Chloroflexus aurantia-cus secretes 3-hydroxypropionate, a possible intermediate in the assim-ilation of CO2 and acetate. Arch. Microbiol. 151, 252-256.
64. Holthuijzen, Y. A., Van Breemen, J. F. L., Konings, W. N., and Van Bruggen, E. F. J. (1986). Elec-tron microscopic studies of car-boxysomes of Thiobacillus neopoli-tanus. Arch. Microbiol. 144, 258-262
65. Huber, H., Gallenberger, M., Jahn, U., Eylert, E., Berg, I. A., Kock-elkorn, D., Eisenreich, W., and Fuchs, G. (2008). A dicarboxylate/4-hydroxybutyrate autotrophic car-bon assimilation cycle in the hyper-thermophilic Archaeum Ignicoccus hospitalis. Proc. Natl. Acad. Sci. U.S.A. 105, 7851-7856.
66. Hugler, M., Huber, H., Molyneaux, S. J., Vetriani, C., and Sievert, S. M. (2007). Autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: evidence for two ways of citrate cleavage. Environ. Microbiol. 9, 81-92.
67. Hugler, M., Petersen, J. M., Dubilier, N., Imhoff, J. F., and Sievert, S. M. (2011). Pathways of carbon and energy metabolism of the epibi-otic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS ONE 6, e16018. doi: 10.1371/jour-nal.pone.0016018
68. Hugler, M., and Sievert, S. M. (2011). Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Ann. Rev. Mar. Sci. 3, 261-289.
69. Hugler, M., Wirsen, C. O., Fuchs, G., Taylor, C. D., and Sievert, S. M. (2005). Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by mem-bers of the epsilon subdivision of proteobacteria. J. Bacteriol. 187, 3020-3027.
70. Imhoff, J. F., Hiraishi, A., and Sul-ing, J. (2005). "Anoxygenic pho-totrophic purple bacteria,"in Bergeys Manual of Systematic Bacteriology, eds D. J. Brenner, N. R. Krieg, and J. T. Staley (New York: Springer), 119-132.
71. Ivanovsky, R. N., Krasilnikova, E. N., and Berg, I. A. (1997). A pro-posed citramalate cycle for acetate assimilation in the purple non-sulfur bacterium Rhodospirillum rubrum. FEMS Microbiol. Lett. 153, 399-404.
72. 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 photosynthe-sis. Nature 464, 1210-1213.
73. Joshi, H. M., and Tabita, F. R. (1996). A global two component signal trans-duction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc. Natl. Acad. Sci. U.S.A. 93, 14515-14520.
74. Kanao, T., Fukui, T., Atomi, H., and Imanaka,T. (2001).ATP-citrate lyase from the green sulfur bacterium Chlorobium limicola is a heteromeric enzyme composed of two distinct gene products. Eur. J. Biochem. 268, 1670-1678.
75. Kaplan, A., and Reinhold, L. (1999). CO2 concentrating mechanisms in photosynthetic microorganisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 539-570.
76. Kawasumi, T., Igarashi, Y., Kodama, T., and Minoda, Y. (1984). Hydrogenobacter thermophilus gen. nov, sp. nov,. an extremely thermophilic, aerobic, hydrogen oxidizing bacterium. Int. J. Syst. Bacteriol. 34, 5-10.
77. Kim, W., and Tabita, F. R. (2006). Both subunits of ATP-citrate lyase from Chlorobium tepidum contribute to catalytic activity. J. Bacteriol. 188, 6544-6552.
78. Klatt, C. G., Bryant, D. A., and Ward, D. M. (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.
79. Knowles, V. L., and Plaxton, W. C. (2003). From genome to enzyme: analysis of key glycolytic and oxidative pentose-phosphate path-way enzymes in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 44, 758-763.
80. Koblizek, M., Beja, O., Bidigare, R. R., Christensen, S., Benitez-Nelson, B., Vetriani, C., Kolber, M. K., Falkowski, P. G., and Kolber, Z. S. (2003). Isolation and characteriza-tion of Erythrobacter sp. strains from the upper ocean. Arch. Microbiol. 180, 327-338.
81. Kolber, Z. S., Plumley, F. G., Lang, A. S., Beatty, J. T., Blankenship, R. E., Van-Dover, C. L., Vetriani, C., Koblizek, M., Rathgeber, C., and Falkowski, P. G. (2001). Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292, 2492-2495.
82. Kondratieva,E. N.,Ivanovsky,R. N.,and Krasilnikova, E. N. (1992). Carbon metabolism in Chloroflexus auran-tiacus. FEMS Microbiol. Lett. 100, 269-271.
83. Kornberg, H. L., and Krebs, H. A. (1957). Synthesis of cell constituents from C2-units by a modified tri-carboxylic acid cycle. Nature 179, 988-991.
84. Korotkova, N., Chistoserdova, L., Kuksa, V., and Lidstrom, M. E. (2002). Glyoxylate regeneration pathway in the methylotroph Methylobacterium extorquens AM1. J. Bacteriol. 184, 1750-1758.
85. Kramer, D. M., Schoepp, B., Liebl, U., and Nitschke, W. (1997). Cyclic elec-tron transfer in Heliobacillus mobilis involving a menaquinol-oxidizing cytochrome bc complex and an RCI-type reaction center. Biochemistry 36, 4203-4211.
86. Krasilnikova, E. N., Keppen, O. I., Gor-lenko, V. M., and Kondrateva, E. N. (1986). Growth of Chloroflexus aurantiacus on media with different organic compounds and pathways of their metabolism. Microbiology 55, 325-329.
87. Krasilnikova, E. N., and Kondrateva, E. N. (1987). Growth of Chloroflexus aurantiacus under anaerobic condi-tions in the dark and the metabolism of organic substrates. Microbiology 56, 281-285.
88. Krebs, H. A., and Johnson,W. A. (1937). The role of citric acid in interme-diate metabolism in animal tissues. Enzymologia 4, 148-156.
89. Kruger, N. J., and von Schaewen, A. (2003). The oxidative pentose phos-phate pathway: structure and organ-isation. Curr. Opin. Plant Biol. 6, 236-246.
90. Kusian,B.,and Bowien,B. (1997). Orga-nization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol. Rev. 21, 135-155.
91. Laguna, R., Tabita, F. R., and Alber, B. E. (2011). Acetate-dependent photoheterotrophic growth and the differential requirement for the Calvin-Benson-Bassham reduc-tive pentose phosphate cycle in Rhodobacter sphaeroides and Rhodopseudomonas palustris. Arch. Microbiol. 193, 151-154.
92. Lamble, H. J., Heyer, N. I., Bull, S. D., Hough, D. W., and Danson, M. J. (2003). Metabolic pathway promis-cuity in the archaeon Sulfolobus solfataricus revealed by studies on glucose dehydrogenase and 2-keto-3-deoxygluconate aldolase. J. Biol. Chem. 278, 34066-34072.
93. Lamzin, V. S., Dauter, Z., and Wilson, K. S. (1995). How nature deals with stereoisomers. Curr. Opin. Struct. Biol. 5, 830-836.
94. Lauble, H., Kennedy, M. C., Emptage, M. H., Beinert, H., and Stout, C. D. (1996). The reaction of fluorocitrate with aconitase and the crystal struc-ture of the enzyme-inhibitor com-plex. Proc. Natl. Acad. Sci. U.S.A. 93, 13699-13703.
95. Levican, G., Ugalde, J. A., Ehrenfeld, N., Maass, A., and Parada, P. (2008). Comparative genomic analysis of carbon and nitrogen assimilation mechanisms in three indigenous bioleaching bacteria: predictions and validations. BMC Genomics 9, 581. doi: 10.1186/1471-2164-9-581
96. Li, F., Hagemeier, C. H., Seedorf, H., Gottschalk, G., and Thauer, R. K. (2007). Re-citrate synthase from Clostridium kluyveri is phylogenet-ically related to homocitrate syn-thase and isopropylmalate synthase rather than to Si-citrate synthase. J. Bacteriol. 189, 4299-4304.
97. Li, Z., Yu, J., Kim, K. R., and Brand, J. (2010). Nitrogen fixa-tion by a marine non-heterocystous cyanobacterium requires a het-erotrophic bacterial consort. Envi-ron. Microbiol. 12, 1185-1193.
98. Lim, S. K., Kim, S. J., Cha, S. H., Oh, Y. K., Rhee, H. J., Kim, M. S., and Lee, J. K. (2009). Complete genome sequence of Rhodobacter sphaeroides KD131. J. Bacteriol. 191, 1118-1119
99. Lindahl, M., and Florencio, F. J. (2003). Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc. Natl. Acad. Sci. U.S.A. 100, 16107-16112.
100. Ljungdahl, L. G. (1986). The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu.Rev.Microbiol.40, 415-450.
101. Lu, Y. K., Marden, J., Han, M., Swingley, W. D.,Mastrian,S. D.,Chowdhury,S. R., Hao, J., Helmy, T., Kim, S., Kur-doglu, A. A., Matthies, H. J., Rollo, D., Stothard, P., Blankenship, R. E., Bauer, C. E., and Touchman, J. W. (2010). Metabolic flexibility revealed in the genome of the cyst-forming alpha-1 proteobacterium Rhodospir-illum centenum. BMC Genomics 11, 325. doi: 10.1186/1471-2164-11-325
102. Madigan, M. T. (2006). "The fam-ily Heliobacteriaceae," in The Prokaryotes, 3rd Edn, Vol. 4, eds M. Dworkin, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (New York: Springer), 951-964.
103. Madigan, M. T., and Jung, D. O. (2009). "An overview of purple bacteria: sys-tematics, physiology, and habitats," in The Purple Phototrophic Bacteria, eds C. N. Hunter, F. Daldal, M. C. Thurnauer, and J. T. Beatty (Dor-drecht: Springer Academic Publish-ers), 1-15.
104. Madigan, M. T., Petersen, S. R., and Brock, T. D. (1974). Nutritional studies on Chloroflexus, a filamen-tous photosynthetic, gliding bac-terium. Arch. Microbiol. 100,97-103
105. Margulis, L. (1968). Evolutionary crite-ria in thallophytes: a radical alterna-tive. Science 161, 1020-1022.
106. McKinlay, J. B., and Harwood, C. S. (2010). Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proc. Natl. Acad. Sci. U.S.A. 107, 11669-11675
107. McKinlay, J. B., and Harwood, C. S. (2011). Calvin cycle flux, pathway constraints, and substrate oxida-tion state together determine the h2 biofuel yield in photoheterotrophic bacteria. MBio 2, e00323-e00310.
108. Moran, M. A., Belas, R., Schell, M. A., Gonzalez, J. M., Sun, F., Sun, S., Binder, B. J., Edmonds, J., Ye, W., Orcutt, B., Howard, E. C., Meile, C., Palefsky, W., Goesmann, A., Ren, Q., Paulsen, I., Ulrich, L. E., Thomp-son, L. S., Saunders, E., and Buchan, A. (2007). Ecological genomics of marine Roseobacter. Appl. Environ. Microbiol. 73, 4559-4569.
109. Morrish, F., Noonan, J., Perez-Olsen, C., Gafken, P. R., Fitzgibbon, M., Kelleher, J., VanGilst, M., and Hock-enbery, D. (2010). Myc-dependent mitochondrial generation of acetyl-CoA contributes to fatty acid biosyn-thesis and histone acetylation during cell cycle entry. J. Biol. Chem. 285, 36267-36274.
110. Nagashima, K. V., Hiraishi, A., Shimada, K., and Matsuura, K. (1997). Hori-zontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J. Mol. Evol. 45, 131-136.
111. Nelson, D. L., and Cox, M. M. (2008). Lehninger Principles of Biochemistry, 5th Edn, New York, NY: W. H. Free-man.
112. Neuera, G., and Bothe, H. (1983). Anaplerotic reactions in Anabaena cylindrica. FEBS Lett. 158, 79-83.
113. Oda,Y., Larimer, F. W., Chain, P. S., Mal-fatti, S., Shin, M. V., Vergez, L. M., Hauser, L., Land, M. L., Braatsch, S., Beatty, J. T., Pelletier, D. A., Schaefer, A. L., and Harwood, C. S. (2008). Multiple genome sequences reveal adaptations of a phototrophic bac-terium to sediment microenviron-ments. Proc. Natl. Acad. Sci. U.S.A. 105, 18543-18548.
114. Owttrim, G. W., and Colman, B. (1988). Phosphoenolpyruvate car-boxylase mediated carbon flow in a cyanobacterium. Biochem. Cell Biol. 66, 93-99.
115. Pace, N. R. (1997). A molecular view of microbial diversity and the bios-phere. Science 276, 734-740.
116. Pandelia, M. E., Nitschke, W., Infossi, P., Giudici-Orticoni, M. T., Bill, E., and Lubitz, W. (2011). Character-ization of a unique [FeS] clus-ter in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus. Proc. Natl. Acad. Sci. U.S.A. 108, 6097-6102.
117. Peyraud, R., Kiefer, P., Christen, P., Mas-sou, S., Portais, J. C., and Vorholt, J. A. (2009). Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc. Natl. Acad. Sci. U.S.A. 106, 4846-4851.
118. Pickett, M. W., Williamson, M. P., and Kelly, D. J. (1994). An enzyme and 13C-NMR of carbon metabolism in heliobacteria. Photosyn. Res. 41, 75-88.
119. Qian, J., Khandogin, J., West, A. H., and Cook, P. F. (2008). Evidence for a catalytic dyad in the active site of homocitrate synthase from Saccha-romyces cerevisiae. Biochemistry 47, 6851-6858.
120. Rathmell, J. C., and Newgard, C. B. (2009). Biochemistry. A glucose-to-gene link. Science 324, 1021-1022.
121. Raven, J. (2009). Contributions of anoxygenic and oxygenic phototro-phy and chemolithotrophy to car-bon and oxygen fluxes in aquatic environments. Aquat. Microb. Ecol. 56, 177-192.
122. Raymond, J., and Blankenship, R. E. (2004). Biosynthetic pathways, gene replacement and the antiquity of life. Geobiology 2, 199-203.
123. Raymond, J., Zhaxybayeva, O., Goga-rten, J. P., Gerdes, S. Y., and Blanken-ship, R. E. (2002). Whole-genome analysis of photosynthetic prokary-otes. Science 298, 1616-1620.
124. Sattley, W. M., and Blankenship, R. E. (2010). Insights into heliobacte-rial photosynthesis and physiology from the genome of Heliobacterium modesticaldum. Photosyn. Res. 104, 113-122.
125. Sattley, W. M., Madigan, M. T., Swing-ley, W. D., Cheung, P. C., Clocksin, K. M., Conrad, A. L., Dejesa, L. C., Honchak, B. M., Jung, D. O., Kar-bach, L. E., Kurdoglu, A., Lahiri, S., Mastrian, S. D., Page, L. E., Taylor, H. L., Wang, Z. T., Raymond, J., Chen, M., Blankenship, R. E., and Touch-man, J. W. (2008). The genome of Heliobacterium modesticaldum,a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J. Bacte-riol. 190, 4687-4696.
126. Say, R. F., and Fuchs, G. (2010). Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464, 1077-1081.
127. Scanlan,D. J.,Sundaram,S.,Newman,J., Mann, N. H., and Carr, N. G. (1995). Characterization of a zwf mutant of Synechococcus sp. strain PCC 7942. J. Bacteriol. 177, 2550-2553.
128. Schneider, G., Lindqvist, Y., and Vihko, P. (1993). Three-dimensional struc-ture of rat acid phosphatase. EMBO J. 12, 2609-2615.
129. Selig, M., Xavier, K. B., Santos, H., and Schonheit, P. (1997). Comparative analysis of Embden-Meyerhof and Entner-Doudoroff glycolytic pathways in hyperther-mophilic archaea and the bacterium Thermotoga. Arch. Microbiol. 167, 217-232.
130. Shastri, A. A., and Morgan, J. A. (2005). Flux balance analysis of photoau-totrophic metabolism. Biotechnol. Prog. 21, 1617-1626.
131. 2 assimilation via the reductive tricarboxylic acid cycle in an obligately autotrophic, aerobic hydrogen oxidizing bacterium, Hydrogenobacter ther-mophilus. Arch. Microbiol. 141, 198-203.
132. Shiba, T. (1991). Roseobacter litoralis gen. nov., sp. nov. and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst. Appl. Microbiol. 14, 140-145.
133. Shiba, T., and Harashima, K. (1986). Aerobic photosynthetic bacteria. Microbiol. Sci. 3, 376-378.
134. Shiba, T., and Simidu, U. (1982). Ery-throbacter longus gen. nov., sp. nov., an aerobic bacterium which contains bacteriochlorophyll a. Int. J. Syst. Bacteriol. 32, 211-217.
135. Sirevag, R. (1995). "Carbon metabo-lism in green bacteria," in Anoxy-genic Photosynthetic Bacteria, eds R. E. Blankenship, M. T. Madigan, and C. E. Bauer (Amsterdam: Kluwer), 871-883.
136. Sirevag, R., and Castenholtz, R. W. (1979). Aspects of carbon metabo-lism in Chloroflexus. Arch. Microbiol. 120, 151-153.
137. Smejkalova, H., Erb, T. J., and Fuchs, G. (2010). Methanol assim-ilation in Methylobacterium extorquens AM1: demonstra-tion of all enzymes and their regulation. PLoS ONE 5, e13001. doi: 10.1371/journal.pone.0013001
138. Smith, A. J. (1982). "Modes of cyanobacterial carbon metabolism," in The Biology of Cyanobacteria, eds N. G. Carr and B. A. Whitton (Oxford: Blackwell Scientific Publi-cations), 47-86.
139. Sorokin, D. Y., Trotsenko, Y. A., Doron-ina, N. V., Tourova, T. P., Galinski, E. A., Kolganova, T. V., and Muyzer, G. (2007). Methylohalomonas lacus gen. nov., sp. nov. and Methy-lonatrum kenyense gen. nov., sp. nov., methylotrophic gammapro-teobacteria from hypersaline lakes. Int. J. Syst. Evol. Microbiol. 57, 2762-2769.
140. Srere, P. A. (1963). Citryl-CoA and the citrate condensing enzyme. Biochim. Biophys. Acta 77, 693-696.
141. Stal, L. J., and Moezelaar, R. (1997). Fer-mentation in cyanobacteria. FEMS Microbiol. Rev. 21, 179-211.
142. Stanier, R. Y., and Cohen-Bazire, G. (1977). "Photosynthetic prokary-otes: the cyanobacteria," in Annual Review of Microbiology, eds M. P. Starr, J. L. Ingraham, and A. Balows (Palo Alto, CA: Annual Reviews Inc.), 225-274.
143. Stockel, J., Jacobs, J. M., Elvitigala, T. R., Liberton, M., Welsh, E. A., Polpitiya, A. D., Gritsenko, M. A., Nicora, C. D., Koppenaal, D. W., Smith, R. D., and Pakrasi, H. B. (2011). Diurnal rhythms result in significant changes in the cellular protein complement in the cyanobacterium cyanothece 51142. PLoS ONE 6, e16680. doi: 10.1371/journal.pone.0016680
144. 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.
145. Strnad, H., Lapidus, A., Paces, J., Ulbrich, P., Vlcek, C., Paces, V., and Haselkorn, R. (2010). Complete genome sequence of the photosyn-thetic purple nonsulfur bacterium Rhodobacter capsulatus SB 1003. J. Bacteriol. 192, 3545-3546.
146. Summers, M. L., Wallis, J. G., Camp-bell, E. L., and Meeks, J. C. (1995). Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. J. Bacteriol. 177, 6184-6194.
147. Sun, T., Hayakawa, K., Bateman, K. S., and Fraser, M. E. (2010). Identifi-cation of the citrate-binding site of human ATP-citrate lyase using X-ray crystallography. J. Biol. Chem. 285, 27418-27428.
148. Swingley, W. D., Sadekar, S., Mastrian, S. D., Matthies, H. J., Hao, J., Ramos, H., Acharya, C. R., Conrad, A. L., Taylor, H. L., Dejesa, L. C., Shah, M. K., OHuallachain, M, E., Lince, M. T., Blankenship, R. E., Beatty, J. T., and Touchman, J. W. (2007). The complete genome sequence of Roseobacter denitrificans reveals a mixotrophic rather than photosyn-thetic metabolism. J. Bacteriol. 189, 683-690.
149. 2 fixa-tion in purple bacteria," in Anoxy-genic Photosynthetic Bacteria, eds R. E. Blankenship, M. T. Madigan, and C. E. Bauer (Amsterdam: Kluwer), 885-914.
150. Takai, K., Campbell, B. J., Cary, S. C., Suzuki, M., Oida, H., Nunoura, T., Hirayama, H., Nakagawa, S., Suzuki, Y., Inagaki, F., and Horikoshi, K. (2005). Enzymatic and genetic char-acterization of carbon and energy metabolisms by deep-sea hydrother-mal chemolithoautotrophic isolates of Epsilonproteobacte-ria. Appl. Environ. Microbiol. 71, 7310-7320.
151. Tang, K. H., Barry, K., Chertkov, O., Dalin, E., Han, C. S., Hauser, L. J., Honchak, B. M., Karbach, L. E., Land, M. L., Lapidus, A., Larimer, F. W., Mikhailova, N., Pitluck, S., Pierson, B. K., and Blankenship, R. E. (2011). Complete genome sequence of the filamentous anoxy-genic phototrophic bacterium Chlo-roflexus aurantiacus. BMC Genomics 12, 334. doi: 10.1186/1471-2164-12-334
152. Tang, K. H., and Blankenship, R. E. (2010). Both forward and reverse TCA cycles operate in green sul-fur bacteria. J. Biol. Chem. 285, 35848-35854.
153. Tang, K. H., Feng, X., Tang, Y. J., and Blankenship, R. E. (2009a). Car-bohydrate metabolism and carbon fixation in Roseobacter denitrificans OCh114. PLoS ONE 4, e7233. doi: 10.1371/journal.pone.0007233
154. Tang, Y. J., Yi, S., Zhuang, W. Q., Zinder, S. H., Keasling, J. D., and Alvarez-Cohen, L. (2009b). Inves-tigation of carbon metabolism in "Dehalococcoides ethenogenes" strain 195 by use of isotopomer and tran-scriptomic analyses. J. Bacteriol. 191, 5224-5231.
155. Tang, K. H., Feng, X., Zhuang, W. Q., Alvarez-Cohen, L., Blankenship, R. E., and Tang, Y. J. (2010a). Car-bon flow of heliobacteria is related more to clostridia than to the green sulfur bacteria. J. Biol. Chem. 285, 35104-35112.
156. Tang, K. H., Yue, H., and Blanken-ship, R. E. (2010b). Energy metabolism of Heliobacterium modesticaldum during pho-totrophic and chemotrophic growth. BMC Microbiol. 10, 150. doi: 10.1186/1471-2180-10-150
157. Thauer, R. K. (2007). Microbiology. A fifth pathway of carbon fixation. Science 318, 1732-1733.
158. Thauer, R. K., Jungermann, K., and Decker, K. (1977). Energy conserva-tion in chemotropic anaerobic bac-teria. Bacteriol. Rev. 41, 100-180.
159. Thauer, R. K., Moller-Zinkhan, D., and Spormann, A. M. (1989). Biochem-istry of acetate catabolism in anaer-obic chemotrophic bacteria. Annu. Rev. Microbiol. 43, 43-67.
160. Tripp, H. J., Bench, S. R., Turk, K. A., Foster, R. A., Desany, B. A., Niazi, F., Affourtit, J. P., and Zehr, J. P. (2010). Metabolic streamlin-ing in an open-ocean nitrogen-fixing cyanobacterium. Nature 464, 90-94
161. Tucci, A. F., and Ceci, L. N. (1972). Homocitrate synthase from yeast. Arch. Biochem. Biophys. 153, 742-750.
162. Voordeckers, J. W., Do, M. H., Hugler, M., Ko, V., Sievert, S. M., and Vetriani, C. (2008). Culture depen-dent and independent analyses of 16S rRNA and ATP citrate lyase genes: a comparison of microbial communities from different black smoker chimneys on the Mid-Atlantic Ridge. Extremophiles 12, 627-640.
163. Wachtershauser, G. (1990). Evolution of the first metabolic cycles. Proc. Natl. Acad. Sci. U.S.A. 87, 200-204.
164. Wahlund, T. M., and Tabita, F. R. (1997). The reductive tricarboxylic acid cycle of carbon dioxide assim-ilation: initial studies and purifi-cation of ATP-citrate lyase from the green sulfur bacterium Chloro-bium tepidum. J. Bacteriol. 179, 4859-4867.
165. Wang, Q., Zhang,Y.,Yang, C., Xiong, H., Lin, Y., Yao, J., Li, H., Xie, L., Zhao, W., Yao, Y., Ning, Z. B., Zeng, R., Xiong, Y., Guan, K. L., Zhao, S., and Zhao, G. P. (2010). Acetylation of metabolic enzymes coordinates car-bon source utilization and metabolic flux. Science 327, 1004-1007.
166. 2 fix-ation in Rhodobacter sphaeroides and Rhodospirillum rubrum in the absence of ribulose bisphosphate carboxylase-oxygenase. J. Bacteriol. 175, 7109-7114.
167. Wellen, K. E., Hatzivassiliou, G., Sachdeva, U. M., Bui, T. V., Cross, J. R., and Thompson, C. B. (2009). ATP-citrate lyase links cel-lular metabolism to histone acetyla-tion. Science 324, 1076-1080.
168. Williams, T. J., Zhang, C. L., Scott, J. H., and Bazylinski, D. A. (2006). Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl. Environ. Microbiol. 72, 1322-1329.
169. Woese,C. R. (1987). Bacterial evolution. Microbiol. Rev. 51, 221-271.
170. Wolk, C. P. (1973). Physiology and cytological chemistry of blue-green algae. Bacteriol. Rev. 37, 32-101.
171. Wood, H. G. (1991). Life with CO or CO2 and H2 as a source of carbon and energy. FASEB J. 5, 156-163.
172. Wulandari, A. P., Miyazaki, J., Kobashi, N., Nishiyama, M., Hoshino, T., and Yamane, H. (2002). Characteriza-tion of bacterial homocitrate syn-thase involved in lysine biosynthesis. FEBS Lett. 522, 35-40.
173. Yang, C., Hua, Q., and Shimizu, K. (2002). Quantitative analysis of intracellular metabolic fluxes using GC-MS and two-dimensional NMR spectroscopy. J. Biosci. Bioeng. 93, 78-87.
174. Yurkov, V., Jappe, J., and Vermeglio, A. (1996). Tellurite resistance and reduction by obligately aerobic pho-tosynthetic bacteria. Appl. Environ. Microbiol. 62, 4195-4198.
175. Yurkov, V. V., and Beatty, J. T. (1998). Aerobic anoxygenic phototrophic bacteria. Microbiol. Mol. Biol. Rev. 62, 695-724.
176. Yurkov, V. V., and Csotonyi, J. T. (2009). "New light on aerobic anoxygenic phototrophs," in The Purple Pho-totrophic Bacteria, eds C. N. Hunter, F. Daldal, M. C. Thurnauer, and J. T. Beatty (Dordrecht: Springer Acade-mic Publishers), 31-55.
177. Yurkov, V. V., Krasilnikova, E. N., and Gorlenko, V. M. (1991). Enzymes Involved in heterotrophic carbon metabolism of aerobic Erythrobac-ter sibiricus and Erythrobacter longus bacteria containing bacte-riochlorophyll a. Microbiology 60, 401-403.
178. Zarzycki, J., Brecht, V., Muller, M., and Fuchs, G. (2009). Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. Proc. Natl. Acad. Sci. U.S.A. 106, 21317-21322.
179. Zehr,J. P.,Bench,S. R.,Carter,B. J.,Hew-son, I., Niazi, F., Shi, T., Tripp, H. J., and Affourtit, J. P. (2008). Glob-ally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxy-genic photosystem II. Science 322, 1110-1112.
180. Zhang, S., Laborde, S. M., Frankel, L. K., and Bricker,T. M. (2004). Four novel genes required for optimal photoau-totrophic growth of the cyanobac-terium Synechocystis sp. strain PCC 6803 identified by in vitro transpo-son mutagenesis. J. Bacteriol. 186, 875-879.
181. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H., Li, Y., Shi, J., An, W., Han-cock, S. M., He, F., Qin, L., Chin, J., Yang, P., Chen, X., Lei, Q., Xiong, Y., and Guan, K. L. (2010). Regula-tion of cellular metabolism by pro-tein lysine acetylation. Science 327, 1000-1004.