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Phototrophic CO2 Fixation: Recent Insights into Ancient Metabolisms

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Functional Genomics and Evolution of Photosynthetic Systems

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 33))

Summary

The production of all (autotrophy) or a substantial proportion (mixotrophy) of newly synthesized biomass from carbon dioxide is a hallmark of plants and a number of bacteria and archaea. Carbon dioxide fixation enables autotrophs to form the basis of entire ecosystem foodwebs as primary producers and mixotrophs to efficiently utilize simple forms of carbon present in various environments. During fixation, CO2 must ultimately be reduced to the level of formaldehyde for assimilation into biomass and, for this reason, CO2 fixation is also utilized by numerous organisms to dispose of excess reducing power. Currently, six distinct CO2 fixation pathways are recognized amongst autotrophic prokaryotes and eukaryotes. The impact of genomics on our understanding of the distribution, function(s), and regulation of these pathways and their unique enzymes will be described as will two recently discovered pathways, one for autotrophic or mixotrophic CO2 fixation in some photosynthetic bacteria and the other for acetate assimilation by a wide range of bacteria, including phototrophs, that involves a novel carboxylation step.

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Abbreviations

3-HP:

3-hydroxypropionate

3-HPP:

3-HP pathway

4-HB:

4-hydroxybenzoate

ACL:

ATP:citrate lyase

CBB cycle:

Calvin-Benson-Bassham cycle

CCL:

citryl CoA synthase

CCS:

citryl CoA lyase

Fd:

Ferredoxin

Fe-S:

Iron sulfur cluster

NSP bacteria:

Nonsulfur purple phototrophic bacteria

ORF:

Open reading frame;

RC1/2:

Reaction center type 1 (Fe-S reducing) or type 2 (quinone reducing)

rTCA:

reductive or reverse TCA cycle

References

  • Akakura R and Winans SC (2002) Constitutive mutations of the OccR regulatory protein affect DNA bending in response to metabolites released from plant tumors. J Biol Chem 277: 5866–5874

    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 

  • Alber B, Olinger M, Rieder A, Kockelkorn D, Jobst B, Hügler M and Fuchs G. (2006a) Malonyl-coenzyme A reductase in the modified 3-hydroxypropionate cycle for autotrophic carbon fixation in archaeal Metallosphaera and Sulfolobus spp. J. Bacteriol 188:8551–8559.

    PubMed  CAS  Google Scholar 

  • Alber BE, Spanheimer R, Ebenau-Jehle C and Fuchs G (2006b) Study of an alternate glyoxylate cycle for acetate assimilation by Rhodobacter sphaeroides. Mol Microbiol 61: 297–309

    PubMed  CAS  Google Scholar 

  • Alber BE, Kung JW and Fuchs G (2008) 3-Hydroxypropionyl-coenzyme A synthetase from Metallosphaera sedula, an enzyme involved in autotrophic CO2 fixation. J Bacteriol 190: 1383–1389

    PubMed  CAS  Google Scholar 

  • Anderson SL and McIntosh L (1991) Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. strain PCC 6803: a blue-light-requiring process. J Bacteriol 173: 2761–2767

    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 

  • Aoshima M (2007) Novel enzyme reactions related to the tricarboxylic acid cycle: Phylogenetic/functional implications and biotechnological applications. Appl Microbiol Biotechnol 75: 249–255

    PubMed  CAS  Google Scholar 

  • Aoshima M, Ishii M and Igarashi Y (2004a) 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

    PubMed  CAS  Google Scholar 

  • Aoshima M, Ishii M and Igarashi Y (2004b) 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bauld J and Brock TD (1973) Ecological studies of Chloroflexus, a gliding photosynthetic bacterium. Arch Mikrobiol 92: 267–284

    Google Scholar 

  • Berg IA, Keppen OI, Krasil’nikova EN, Ugol’kova NV and Ivanovsky RN (2005) Carbon metabolism of filamentous anoxygenic phototrophic bacteria of the family Oscillochloridaceae. Microbiology 74: 258–264

    CAS  Google Scholar 

  • Berg IA, Kockelkorn D, Buckel W and Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318: 1782–1786

    PubMed  CAS  Google Scholar 

  • Bott M and Dimroth P (1994) Klebsiella pneumoniae genes for citrate lyase and citrate lyase ligase: Localization, sequencing, and expression. Mol Microbiol 14: 347–356

    PubMed  CAS  Google Scholar 

  • Buchan A, Gonzalez JM and Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71: 5665–5677

    PubMed  CAS  Google Scholar 

  • Buick R (2008) When did oxygenic photosynthesis evolve? Philos Trans R Soc Lond B Biol Sci 363: 2731–2743

    PubMed  CAS  Google Scholar 

  • Campbell BJ, Engel AS, Porter ML and Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458–468

    PubMed  CAS  Google Scholar 

  • Cleaves HJ, Chalmers JH, Lazcano A, Miller SL and Bada JL (2008) A reassessment of prebiotic organic synthesis in neutral planetary atmospheres. Orig Life Evol Biosph 38: 105–115

    PubMed  CAS  Google Scholar 

  • Comolli JC, Carl AJ, Hall C and Donohue T (2002) Transcriptional activation of the Rhodobacter sphaeroides cytochrome c2 gene P2 promoter by the response regulator PrrA. J Bacteriol 184: 390–399

    PubMed  CAS  Google Scholar 

  • Cunchillos C and Lecointre G (2007) Ordering events of biochemical evolution. Biochimie 89: 555–573

    PubMed  CAS  Google Scholar 

  • Dangel AW and Tabita FR (2009) Protein-protein interactions between CbbR and RegA (PrrA), transcriptional regulators of the cbb operons of Rhodobacter sphaeroides. Mol Microbiol 71: 717–729

    PubMed  CAS  Google Scholar 

  • Dangel AW, Gibson JL, Janssen AP and Tabita FR (2005) Residues that influence in vivo and in vitro CbbR function in Rhodobacter sphaeroides and identification of a specific region critical for co-inducer recognition. Mol Microbiol 57: 1397–1414

    PubMed  CAS  Google Scholar 

  • Dubbs JM and Tabita FR (1998) Two functionally distinct regions upstream of the cbb I operon of Rhodobacter sphaeroides regulate gene expression. J Bacteriol 180: 4903–4911

    PubMed  CAS  Google Scholar 

  • Dubbs JM and Tabita FR (2003) Interactions of the cbb II promoter-operator region with CbbR and RegA (PrrA) regulators indicate distinct mechanisms to control expression of the two cbb operons of Rhodobacter sphaeroides. J Biol Chem 278: 16443–16450

    PubMed  CAS  Google Scholar 

  • Dubbs JM and Tabita FR (2004) Regulators of nonsulfur purple phototrophic bacteria and the interactive control of CO2 assimilation, nitrogen fixation, hydrogen metabolism and energy generation. FEMS Microbiol Rev 28: 353–376

    PubMed  CAS  Google Scholar 

  • Dubbs JM, Bird TH, Bauer CE and Tabita FR (2000) Interaction of CbbR and RegA* transcription regulators with the Rhodobacter sphaeroides cbb I promoter-operator region. J Biol Chem 275: 19224–19230

    PubMed  CAS  Google Scholar 

  • Dubbs P, Dubbs JM and Tabita FR (2004) Effector-mediated interaction of CbbRI and CbbRII regulators with target sequences in Rhodobacter capsulatus. J Bacteriol 186: 8026–8035

    PubMed  CAS  Google Scholar 

  • Edgren T and Nordlund S (2006) Two pathways of electron transport to nitrogenase in Rhodospirillum rubrum: The major pathway is dependent on the fix gene products. FEMS Microbiol Lett 260: 30–35

    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 

  • el-Refai AH, Nashat MA and Salem HM (1974) Heterotrophic growth of the nitrogen fixing blue-green alga Nostoc ­muscorum. Z Allg Mikrobiol 14: 297–302

    PubMed  CAS  Google Scholar 

  • Elsen S, Swem LR, Swem DL and Bauer CE (2004) RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbiol Mol Biol Rev 68: 263–279

    PubMed  CAS  Google Scholar 

  • Emmerich R, Panglungtshang K, Strehler P, Hennecke H and Fischer HM (1999) Phosphorylation, dephosphorylation and DNA-binding of the Bradyrhizobium japonicum RegSR two-component regulatory proteins. Eur J Biochem 263: 455–463

    PubMed  CAS  Google Scholar 

  • Erb TJ, Berg IA, Brecht V, Müller M, Fuchs G and Alber BE (2007) Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: The ethylmalonyl-CoA pathway. Proc Natl Acad Sci USA 104: 10631–10636

    PubMed  CAS  Google Scholar 

  • Erb TJ, Retey J, Fuchs G and Alber BE (2008) Ethylmalonyl-CoA mutase from Rhodobacter sphaeroides defines a new subclade of coenzyme B12-dependent acyl-CoA mutases. J Biol Chem 283: 32283–32293

    PubMed  CAS  Google Scholar 

  • Erb TJ, Brecht V, Fuchs G, Müller M and Alber BE (2009a) Carboxylation mechanism and stereochemistry of crotonyl-CoA carboxylase/reductase. Proc Natl Acad Sci USA 106: 8871–8876

    PubMed  CAS  Google Scholar 

  • Erb TJ, Fuchs G and Alber BE (2009b) (2S)-Methylsuccinyl-CoA dehydrogenase closes the ethylmalonyl-CoA pathway for acetyl-CoA assimilation. Mol Microbiol 73: 992–1008

    Google Scholar 

  • Erb TJ, Frerichs-Revermann L, Fuchs G and Alber BE (2010) The apparent malate synthase activity of Rhodobacter sphaeroides is due to two paralogous enzymes, (3S)-malyl-coenzyme A (CoA)/β-methylmalyl-CoA lyase and (3S)-malyl-CoA thioesterase. J Bacteriol 192: 1249–1258

    Google Scholar 

  • Evans MC, Buchanan BB and Arnon DI (1966) A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA 55: 928–934

    PubMed  CAS  Google Scholar 

  • Ezezika OC, Haddad S, Clark TJ, Neidle EL and Momany C (2007) Distinct effector-binding sites enable synergistic transcriptional activation by BenM, a LysR-type regulator. J Mol Biol 367: 616–629

    PubMed  CAS  Google Scholar 

  • Falcone DL and Tabita FR (1991) Expression of endogenous and foreign ribulose 1,5-bisphosphate carboxylase-oxygenase (Rubisco) genes in a Rubisco deletion mutant of Rhodobacter sphaeroides. J Bacteriol 173: 2099–2108

    PubMed  CAS  Google Scholar 

  • Fales L, Kryszak L and Zeilstra-Ryalls J (2001) Control of hemA expression in Rhodobacter sphaeroides 2.4.1: Effect of a transposon insertion in the hbdA gene. J Bacteriol 183: 1568–1576

    PubMed  CAS  Google Scholar 

  • Feisthauer S, Wick LY, Kastner M, Kaschabek SR, Schlomann M and Richnow HH (2008) Differences of heterotrophic 13CO2 assimilation by Pseudomonas knackmussii strain B13 and Rhodococcus opacus 1CP and potential impact on biomarker stable isotope probing. Environ Microbiol 10: 1641–1651

    PubMed  CAS  Google Scholar 

  • Finn MW and Tabita FR (2003) Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea. J Bacteriol 185: 3049–3059

    PubMed  CAS  Google Scholar 

  • Friedmann S, Steindorf A, Alber BE and Fuchs G (2006) 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, 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 NU, Martinez A, Mincer TJ and DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic bacteria and archaea. Nature 439: 847–850

    PubMed  CAS  Google Scholar 

  • Gibson JL (1995) Genetic analysis of CO2 fixation genes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria pp 1107–1124. Kluwer, Dordrecht

    Google Scholar 

  • Gibson JL and Tabita FR (1993) Nucleotide sequence and functional analysis of cbbR, a positive regulator of the Calvin cycle operons of Rhodobacter sphaeroides. J Bacteriol 175: 5778–5784

    PubMed  CAS  Google Scholar 

  • Gibson JL and Tabita FR (1996) The molecular regulation of the reductive pentose phosphate pathway in proteobacteria and cyanobacteria. Arch Microbiol 166: 141–150

    PubMed  CAS  Google Scholar 

  • Gonzalez JM and Moran MA (1997) Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol 63: 4237–4242

    PubMed  CAS  Google Scholar 

  • Graves DA, Spradlin GM and Greenbaum E (1990) Effect of oxygen on photoautotrophic and heterotrophic growth of Chlamydomonas reinhardtii in an anoxic atmosphere. Photochem Photobiol 52: 585–590

    PubMed  CAS  Google Scholar 

  • Greene DN, Whitney SM and Matsumura I (2007) Artificially evolved Synechococcus PCC6301 Rubisco variants exhibit improvements in folding and catalytic efficiency. Biochem J 404: 517–524

    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 

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

    PubMed  CAS  Google Scholar 

  • Heinnickel M and Golbeck JH (2007) Heliobacterial photosynthesis. Photosynth Res 92: 35–53

    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 (2002) 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 

  • Holo H (1989) Chloroflexus aurantiacus secretes 3-hydroxypropionate, a possible intermediate in the assimilation of CO2 and acetate. Arch Microbiol 151: 252–256

    CAS  Google Scholar 

  • Holo H and Sirevag R (1986) Autotrophic growth and CO2 fixation of Chloroflexus aurantiacus. Arch Microbiol 145: 173–180

    CAS  Google Scholar 

  • Hughes NJ, Clayton CL, Chalk PA and Kelly DJ (1998) Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate:acceptor oxidoreductases which mediate electron transport to NADP. J Bacteriol 180: 1119–1128

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hugler M, Huber H, Molyneaux SJ, Vetriani C and Sievert SM (2007) Autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: Evidence for two ways of citrate cleavage. Environl Microbiol 9: 81–92

    PubMed  CAS  Google Scholar 

  • Imker HJ, Fedorov AA, Fedorov EV, Almo SC and Gerlt JA (2007) Mechanistic diversity in the RubisCO superfamily: The “enolase” In the methionine salvage pathway in Geobacillus kaustophilus. Biochemistry 46: 4077–4089

    PubMed  CAS  Google Scholar 

  • Imker HJ, Singh J, Warlick BP, Tabita FR and Gerlt JA (2008) Mechanistic diversity in the RubisCO superfamily: a novel isomerization reaction catalyzed by the RubisCO-like protein from Rhodospirillum rubrum. Biochemistry 47: 11171–11173

    PubMed  CAS  Google Scholar 

  • Inoue K, Kouadio JL, Mosley CS and Bauer CE (1995) Isolation and in vitro phosphorylation of sensory transduction components controlling anaerobic induction of light harvesting and reaction center gene expression in Rhodobacter capsulatus. Biochemistry 34: 391–396

    PubMed  CAS  Google Scholar 

  • Ivanovsky RN, Sintsov NV and Kondratieva EN (1980) ATP-linked citrate lyase activity in the green sulfur bacterium Chlorobium limicola forma thiosulfatophilum. Arch Microbiol 128: 239–241

    Google Scholar 

  • Ivanovsky RN, Fal YI, Berg IA, Ugolkova NV, Krasilnikova 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 trichoides strain DG-6. Microbiology 145: 1743–1748

    PubMed  CAS  Google Scholar 

  • Iverson TM (2006) Evolution and unique bioenergetic mechanisms in oxygenic photosynthesis. Curr Opin Chem Biol 10: 91–100

    PubMed  CAS  Google Scholar 

  • Johnson AP, Cleaves HJ, Dworkin JP, Glavin DP, Lazcano A and Bada JL (2008) The Miller volcanic spark discharge experiment. Science 322: 404

    PubMed  CAS  Google Scholar 

  • Joshi HM and Tabita FR (1996) A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc Natl Acad Sci USA 93: 14515–14520

    PubMed  CAS  Google Scholar 

  • Joshi HM and Tabita FR (2000) Induction of carbon monoxide dehydrogenase to facilitate redox balancing in a ribulose bisphosphate carboxylase/oxygenase-deficient mutant strain of Rhodospirillum rubrum. Arch Microbiol 173: 193–199

    PubMed  CAS  Google Scholar 

  • Joshi GS, Romagnoli S, Verberkmoes NC, Hettich RL, Pelletier D and Tabita FR (2009) Differential accumulation of form I RubisCO in Rhodopseudomonas palustris CGA010 under photoheterotrophic growth conditions with reduced carbon sources. J Bacteriol 191: 4243–4250

    PubMed  CAS  Google Scholar 

  • Joshi GS, Bobst CE and Tabita FR (2011) Unraveling the regulatory twist – regulation of CO2 fixation in Rhodopseudomonas palustris CGA010 mediated by atypical response regulators. Mol Microbiol 80: 756–771

    Google Scholar 

  • Kaihovaara P, Hook-Nikanne J, Uusi-Oukari M, Kosunen TU and Salaspuro M (1998) Flavodoxin-dependent pyruvate oxidation, acetate production and metronidazole reduction by Helicobacter pylori. J Antimicrob Chemother 41: 171–177

    PubMed  CAS  Google Scholar 

  • Kalapos MP (2007) The energetics of the reductive citric acid cycle in the pyrite-pulled surface metabolism in the early stage of evolution. J Theor Biol 248: 251–258

    PubMed  CAS  Google Scholar 

  • Kaneo T, Fukui T, Atomi H, Imanaka T (2001) ATP-citrate lyase from the green sulfur bacterium Chlorobium limicola is a heterodimeric enzyme composed of two distinct gene products. Eur J Biochem 268: 1670–1678

    Google Scholar 

  • Kim W and Tabita FR (2006) Both subunits of ATP-citrate lyase from Chlorobium tepidum contribute to catalytic activity. J Bacteriol 188: 6544–6552

    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 

  • Koblizek M, Beja O, Bidigare RR, Christensen S, Benitez-Nelson B, Vetriani C, Kolber MK, Falkowski PG and Kolber ZS (2003) Isolation and characterization of Erythrobacter sp. strains from the upper ocean. Arch Microbiol 180: 327–338

    PubMed  CAS  Google Scholar 

  • Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C and Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292: 2492–2495

    PubMed  CAS  Google Scholar 

  • Kornberg HL and Krebs HA (1957) Synthesis of cell constituents from C2-units by a modified tricarboxylic acid cycle. Nature 179: 988–991

    PubMed  CAS  Google Scholar 

  • Kranz RG, Gabbert KK, Locke TA and Madigan MT (1997) Polyhydroxyalkanoate production in Rhodobacter capsulatus: Genes, mutants, expression, and physiology. Appl Environ Microbiol 63: 3003–3009

    PubMed  CAS  Google Scholar 

  • Krasilnikova EN, Keppen OI, Gorlenko VM and Kondrateva EN (1986) Growth of Chloroflexus aurantiacus on media with different organic-compounds and pathways of their metabolism. Microbiology 55: 325–329

    Google Scholar 

  • Laguna R, Joshi GS, Dangel AW, Luther AK and Tabita FR (2010) Integrative control of carbon, nitrogen, hydrogen and sulfur metabolism: the central role of the Calvin-Benson-Bassham cycle. Adv Exp Med Biol 675: 265–271

    Google Scholar 

  • Li H, Sawaya MR, Tabita FR and Eisenberg D (2005) Crystal structure of a Rubisco-like protein from the green sulfur bacterium Chlorobium tepidum. Structure 13: 779–789

    PubMed  CAS  Google Scholar 

  • Lindblad A, Jansson J, Brostedt E, Johansson M, Hellman U and Nordlund S (1996) Identification and sequence of a nifJ-like gene in Rhodospirillum rubrum: partial characterization of a mutant unaffected in nitrogen fixation. Mol Microbiol 20: 559–568

    PubMed  CAS  Google Scholar 

  • Lochowska A, Iwanicka-Nowicka R, Plochocka D and Hryniewicz MM (2001) Functional dissection of the LysR-type CysB transcriptional regulator. Regions important for DNA binding, inducer response, oligomerization, and positive control. J Biol Chem 276: 2098–2107

    PubMed  CAS  Google Scholar 

  • Lozier RH, Bogomolni RA and Stoeckenius W (1975) Bacteriorhodopsin: A Light-Driven Proton Pump in Halobacterium halobium. Biophys J 15: 955–962

    PubMed  CAS  Google Scholar 

  • Madigan MT and Gest H (1979) Growth of the photosynthetic bacterium Rhodopseudomonas capsulata chemoautotrophically in darkness with H2 as the energy source. J Bacteriol 137: 524–530

    PubMed  CAS  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 

  • Martin W and Russell MJ (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Philos Trans R Soc Lond B Biol Sci 362: 1887–1925

    PubMed  CAS  Google Scholar 

  • Meister M, Saum S, Alber BE and Fuchs G (2005) L-malyl-coenzyme a/beta-methylmalyl-coenzyme a lyase is involved in acetate assimilation of the isocitrate lyase-negative bacterium Rhodobacter capsulatus. J Bacteriol 187: 1415–1425

    PubMed  CAS  Google Scholar 

  • Menendez C, Bauer Z, Huber H, Gad’on N, Stetter KO and Fuchs G (1999) Presence of acetyl coenzyme a (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J Bacteriol 181: 1088–1098

    PubMed  CAS  Google Scholar 

  • Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117: 528–529

    PubMed  CAS  Google Scholar 

  • Muraoka S, Okumura R, Ogawa N, Nonaka T, Miyashita K and Senda T (2003) Crystal structure of a full-length LysR-type transcriptional regulator, CbnR: unusual combination of two subunit forms and molecular bases for causing and changing DNA bend. J Mol Biol 328: 555–566

    PubMed  CAS  Google Scholar 

  • Olson JM (2006) Photosynthesis in the Archean era. Photosynth Res 88: 109–117

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Oparin AI (1950) [Noncellular form of life and the origin of cells.]. Vestn Akad Med Nauk SSSR 20: 118–122

    PubMed  CAS  Google Scholar 

  • Orgel LE (2008) The implausibility of metabolic cycles on the prebiotic earth. PLoS Biol 6: e18

    PubMed  Google Scholar 

  • Paoli GC and Tabita FR (1998) Aerobic chemolithoautotrophic growth and Rubisco function in Rhodopseu­domonas capsulata and a spontaneous gain of function mutant of Rhodobacter sphaeroides. Arch Microbiol 170: 8–17

    PubMed  CAS  Google Scholar 

  • Paoli GC, Vichivanives P and Tabita FR (1998) Physiological control and regulation of the Rhodobacter capsulatus cbb operons. J Bacteriol 180: 4258–4269

    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 

  • Qian Y and Tabita FR (1996) A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter sphaeroides. J Bacteriol 178: 12–18

    PubMed  CAS  Google Scholar 

  • Ranson-Olson B, Jones DF, Donohue TJ and Zeilstra-Ryalls JH (2006) In vitro and in vivo analysis of the role of PrrA in Rhodobacter sphaeroides 2.4.1 hemA gene expression. J Bacteriol 188: 3208–3218

    PubMed  CAS  Google Scholar 

  • Romagnoli S and Tabita FR (2006) A novel three-protein two-component system provides a regulatory twist on an established circuit to modulate expression of the cbb I region of Rhodopseudomonas palustris CGA010. J Bacteriol 188: 2780–2791

    PubMed  CAS  Google Scholar 

  • Romagnoli S and Tabita FR (2007) Phosphotransfer reactions of the CbbRRS three-protein two- component system from Rhodopseudomonas palustris CGA010 appear to be controlled by an internal molecular switch on the sensor kinase. J Bacteriol 189: 325–335

    PubMed  CAS  Google Scholar 

  • Romagnoli S and Tabita FR (2009) Carbon dioxide metabolism and its regulation in nonsulfur purple photosynthetic bacteria. In: Hunter CN, Daldal F, Thurnauer MC and Beatty JT (eds) The purple phototrophic bacteria, pp 563–576. Springer, Dordrecht, The Netherlands

    Google Scholar 

  • Roslev P, Larsen MB, Jorgensen D and Hesselsoe M (2004) Use of heterotrophic CO2 assimilation as a measure of metabolic activity in planktonic and sessile bacteria. J Microbiol Methods 59: 381–393

    PubMed  CAS  Google Scholar 

  • Rothschild LJ (2008) The evolution of photosynthesis…again? Philos Trans R Soc Lond B Biol Sci 363: 2787–2801

    PubMed  CAS  Google Scholar 

  • Satagopan S, Scott SS, Smith TG and Tabita FR (2009) A Rubisco mutant that confers growth under a normally “inhibitory” oxygen concentration. Biochemistry 48:9076–9083

    Google Scholar 

  • Smirnova IA, Dian C, Leonard GA, McSweeney S, Birse D and Brzezinski P (2004) Development of a bacterial biosensor for nitrotoluenes: The crystal structure of the transcriptional regulator DntR. J Mol Biol 340: 405–418

    PubMed  CAS  Google Scholar 

  • Smith SA and Tabita FR (2002) Up-regulated expression of the cbb(I) and cbb(II) operons during photoheterotrophic growth of a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion mutant of Rhodobacter sphaeroides. J Bacteriol 184: 6721–6724

    PubMed  CAS  Google Scholar 

  • Smith SA and Tabita FR (2003) Positive and negative selection of mutant forms of prokaryotic (cyanobacterial) ribulose-1,5-bisphosphate carboxylase/oxygenase. J Mol Biol 331: 557–569

    PubMed  CAS  Google Scholar 

  • Smith SA and Tabita FR (2004) Glycine 176 affects catalytic properties and stability of the Synechococcus sp. strain PCC6301 ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 279: 25632–25637

    PubMed  CAS  Google Scholar 

  • Srinivasan V and Morowitz HJ (2006) Ancient genes in contemporary persistent microbial pathogens. Biol Bull 210: 1–9

    PubMed  CAS  Google Scholar 

  • Stams AJ and Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7: 568–577

    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 

  • Strauss G, Eisenreich W, Bacher A and Fuchs G (1992) 13C-NMR study of autotrophic CO2 fixation pathways in the sulfur-reducing archaebacterium Thermoproteus neutrophilus and in the phototrophic eubacterium Chloroflexus aurantiacus. Eur J Biochem 205: 853–866

    PubMed  CAS  Google Scholar 

  • Summers ML, Wallis JG, Campbell EL and Meeks JC (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

    PubMed  CAS  Google Scholar 

  • Swingley WD, Sadekar S, Mastrian SD, Matthies HJ, Hao J, Ramos H, Acharya CR, Conrad AL, Taylor HL, Dejesa LC, Shah MK, O’Huallachain M E, 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, Hanson TE, Li H, Satagopan S, Singh J and Chan S (2007) Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev 71: 576–599

    PubMed  CAS  Google Scholar 

  • Tabita FR, Hanson TE, Satagopan S, Witte BH and Kreel NE (2008a) Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Philos Trans R Soc Lond B Biol Sci 363: 2629–2640

    PubMed  CAS  Google Scholar 

  • Tabita FR, Satagopan S, Hanson TE, Kreel NE and Scott SS (2008b) Distinct form I, II, III, and IV RubisCO proteins from the three kingdoms of life provide clues about RubisCO evolution and structure/function relationships. J Exp Bot 59: 1515–1524

    PubMed  CAS  Google Scholar 

  • Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, Hirayama H, Nakagawa S, Suzuki Y, Inagaki F and Horikoshi K (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of epsilonproteobacteria. Appl Environ Microbiol 71: 7310–7320

    PubMed  CAS  Google Scholar 

  • Teufel R, Kung JW, Kockelkorn D, Alber BE and Fuchs G (2009) 3-Hydroxypropionyl-coenzyme A dehydratase and acryloyl-coenzyme A reductase, enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in Sulfolobales. J Bacteriol 191: 4572–4581

    PubMed  CAS  Google Scholar 

  • Thauer RK (2007) Microbiology. A fifth pathway of carbon fixation. Science 318: 1732–1733

    PubMed  CAS  Google Scholar 

  • Tichi MA and Tabita FR (2000) Maintenance and control of redox poise in Rhodobacter capsulatus strains deficient in the Calvin-Benson-Bassham pathway. Arch Microbiol 174: 322–333

    PubMed  CAS  Google Scholar 

  • Tichi MA and Tabita FR (2002) Metabolic signals that lead to control of cbb gene expression in Rhodobacter capsulatus. J Bacteriol 184: 1905–1915

    PubMed  CAS  Google Scholar 

  • van der Meer MT, 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 

  • Vichivanives P, Bird TH, Bauer CE and Tabita FR (2000) Multiple regulators and their interactions in vivo and its in vitro with the cbb regulons of Rhodobacter capsulatus. J Mol Biol 300: 1079–1099

    PubMed  CAS  Google Scholar 

  • Voordeckers JW, Do MH, Hugler M, Ko V, Sievert SM and Vetriani C (2008) Culture dependent 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

    PubMed  CAS  Google Scholar 

  • Wachtershauser G (1988) Before enzymes and templates: theory of surface metabolism. Microbiol Rev 52: 452–484

    PubMed  CAS  Google Scholar 

  • Wachtershauser G (1990) Evolution of the first metabolic cycles. Proc Natl Acad Sci USA 87: 200–204

    PubMed  CAS  Google Scholar 

  • Wahlund TM and Tabita FR (1997) The reductive tricarboxylic acid cycle of carbon dioxide assimilation: Initial studies and purification of ATP-citrate lyase from the green sulfur bacterium Chlorobium tepidum. J Bacteriol 179: 4859–4867.

    PubMed  CAS  Google Scholar 

  • Wang X, Falcone DL and Tabita FR (1993) Reductive pentose phosphate-independent CO2 fixation in Rhodobacter sphaeroides and evidence that ribulose bisphosphate carboxylase/oxygenase activity serves to maintain the redox balance of the cell. J Bacteriol 175: 3372–3379

    PubMed  CAS  Google Scholar 

  • Williams TJ, Zhang CL, Scott JH and Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 72: 1322–1329

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K, Eisen JA, Heidelberg KB, Manning G, Li W, Jaroszewski L, Cieplak P, Miller CS, Li H, Mashiyama ST, Joachimiak MP, van Belle C, Chandonia JM, Soergel DA, Zhai Y, Natarajan K, Lee S, Raphael BJ, Bafna V, Friedman R, Brenner SE, Godzik A, Eisenberg D, Dixon JE, Taylor SS, Strausberg RL, Frazier M and Venter JC (2007) The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol 5: e16

    PubMed  Google Scholar 

  • Yoshida S, Inui M, Yukawa H, Kanao T, Tomizawa K, Atomi H and Imanaka T (2006) Phototrophic growth of a Rubisco-deficient mesophilic purple nonsulfur bacterium harboring a type III Rubisco from a hyperthermophilic archaeon. J Biotechnol 124: 532–544

    PubMed  CAS  Google Scholar 

  • Zarzycki J, Schlichting A, Strychalsky N, Muller M, Alber BE and Fuchs G (2008) Mesaconyl-coenzyme a hydratase, a new enzyme of two central carbon metabolic pathways in bacteria. J Bacteriol 190: 1366–1374

    PubMed  CAS  Google Scholar 

  • Zarzycki J, Brecht V, Müller M and Fuchs G (2009) Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. Proc Natl Acad Sci USA 106: 21317–21322

    Google Scholar 

  • Zerkle AL, House CH and Brantley SL (2005) Biogeochemical signatures through time as inferred from whole microbial genomes. Am J Sci 305: 467–502

    CAS  Google Scholar 

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Acknowledgments

TEH was supported by a CAREER award from the National Science Foundation (MCB-0447649). BEA would like to thank G. Fuchs (Albert-Ludwigs Universität Freiburg) for continuous support. Research on the ethylmalonyl-CoA pathway was supported by DFG grant AL677/1-1 and NSF grant MCB-0842892. FRT was supported by DOE grants DE-FG02-07ER64489 and DE-FG02-08ER15976.

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Authors and Affiliations

  1. College of Earth, Ocean and Environment, Department of Biological Sciences and Delaware Biotechnology Institute, University of Delaware, 127 DBI, 15 Innovation Way, Newark, DE, 19711, USA

    Thomas E. Hanson

  2. Department of Microbiology, The Ohio State University, 484 West 12th Avenue, Columbus, OH, 43210-1292, USA

    Birgit E. Alber

  3. Department of Microbiology and The Plant Molecular Biology Biology/Biotechnology Program, The Ohio State University, 484 West 12th Avenue, Columbus, OH, 43210-1292, USA

    F. Robert Tabita

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  1. Thomas E. Hanson
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  2. Birgit E. Alber
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  3. F. Robert Tabita
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Correspondence to Thomas E. Hanson .

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  1. Dept. Microbiology & Molecular Genetics, Oklahoma State University, Stillwater, 74075, Oklahoma, USA

    Robert Burnap

  2. School of Life Sciences &, Center for Bioenergy & Photosynthesis, Arizona State University, Tempe, 85287-4501, Arizona, USA

    Wim Vermaas

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Hanson, T.E., Alber, B.E., Tabita, F.R. (2012). Phototrophic CO2 Fixation: Recent Insights into Ancient Metabolisms. 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_9

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