Planta

, Volume 237, Issue 2, pp 619–635 | Cite as

Ferredoxin:thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria

  • Monica Balsera
  • Estefania Uberegui
  • Dwi Susanti
  • Ruth A. Schmitz
  • Biswarup Mukhopadhyay
  • Peter Schürmann
  • Bob B. Buchanan
Original Article

Abstract

Uncovered in studies on photosynthesis 35 years ago, redox regulation has been extended to all types of living cells. We understand a great deal about the occurrence, function, and mechanism of action of this mode of regulation, but we know little about its origin and its evolution. To help fill this gap, we have taken advantage of available genome sequences that make it possible to trace the phylogenetic roots of members of the system that was originally described for chloroplasts—ferredoxin, ferredoxin:thioredoxin reductase (FTR), and thioredoxin as well as target enzymes. The results suggest that: (1) the catalytic subunit, FTRc, originated in deeply rooted microaerophilic, chemoautotrophic bacteria where it appears to function in regulating CO2 fixation by the reverse citric acid cycle; (2) FTRc was incorporated into oxygenic photosynthetic organisms without significant structural change except for addition of a variable subunit (FTRv) seemingly to protect the Fe–S cluster against oxygen; (3) new Trxs and target enzymes were systematically added as evolution proceeded from bacteria through the different types of oxygenic photosynthetic organisms; (4) an oxygenic type of regulation preceded classical light–dark regulation in the regulation of enzymes of CO2 fixation by the Calvin–Benson cycle; (5) FTR is not universally present in oxygenic photosynthetic organisms, and in certain early representatives is seemingly functionally replaced by NADP-thioredoxin reductase; and (6) FTRc underwent structural diversification to meet the ecological needs of a variety of bacteria and archaea.

Keywords

Archaea Calvin–Benson cycle Oxidative regulation Phosphoribulokinase Redox regulation Reverse citric acid cycle 

Abbreviations

CB

Calvin–Benson cycle

FBPase

Fructose-1,6-bisphosphatase

Fdx

Ferredoxin

FTS

Ferredoxin/thioredoxin system

FTR

Ferredoxin:thioredoxin reductase

G6PDH

Glucose-6-phosphate dehydrogenase

NADP-MDH

NADP-malate dehydrogenase

NTR

NADP-thioredoxin reductase

NTS

NADP/thioredoxin system

PFOR

Pyruvate:ferredoxin oxidoreductase

PRK

Phosphoribulokinase

RCA

Reverse citric acid cycle

ROS

Reactive oxygen species

SBPase

Sedoheptulose-1,7-bisphosphatase

Trx

Thioredoxin

WL

Wood-Ljundahl

Notes

Acknowledgments

This work was supported by NSF grant MCB # 1020458 to B.M. and B.B.B, and Ministerio de Economía y Competetividad grant number BFU2010-18252 to M.B. E.U. acknowledges support by CSIC Jae-Pre Program. D.S. was supported by NASA Astrobiology: Exobiology and Evolutionary Biology grants NNG05GP24G and NNX09AV28G to B.M. D.S. also received a graduate fellowship from the Virginia Tech Genetics, Bioinformatics and Computational Biology Ph.D. Program. B.B.B. gratefully acknowledges support from an Alexander von Humboldt Research Award that catalyzed the launching of this project at the Ludwig Maximilians University of Munich.

Supplementary material

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Table presence/absence: FTR, NTR and PRK Among the Archaea, FTRc homologs were from Euryarcheota, and were not identified in genomes representing Crenarchaeota or other archaea phyla. Within Euryarcheota, homologs of FTRc were found in some members of archaeoglobi, most methanobacteria and all sequenced methanomicrobia genomes; a single representative was detected in methanococci. FTRc homologs were detected in early and later branching phyla of eubacteria with representatives in aquificae, chloroflexi, spirochaetes, firmicutes, planctomycetes, nitrospirae and the delta-, epsilon- and zeta-classes of the Proteobacteria. A single representative was identified in chlorobi. In cyanobacteria, FTRc was absent in the genomes of Gloeobacter and Prochlorococcus. Distantly related homologs were detected in Clostridia class of the Firmicutes and in two phages from clostridium strains C-Stockholm and D-1873. In eukarya, FTRc is just present in oxyphotosynthetic organisms as a consequence of the endosymbiotic event. Curiously, we have detected in the databases a single representative in a tick (Amblyomma maculatum). Grx-related genes to groups V and VI are indicated in the adjacent column (refer to main body text). The genomes of the organisms included in the list were also checked for the presence of NTR and PRK (columns Q and R, respectively). Some metabolic features of the organisms highlighted with a green background are discussed in Table III. The asterisk refers to incomplete genomes (n.d., non-determined) (XLSX 37 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Monica Balsera
    • 1
  • Estefania Uberegui
    • 1
  • Dwi Susanti
    • 2
    • 3
  • Ruth A. Schmitz
    • 4
  • Biswarup Mukhopadhyay
    • 2
    • 5
  • Peter Schürmann
    • 6
  • Bob B. Buchanan
    • 7
  1. 1.Instituto de Recursos Naturales y Agrobiología de Salamanca (IRNASA-CSIC)SalamancaSpain
  2. 2.Virginia Bioinformatics Institute, Virginia TechBlacksburgUSA
  3. 3.Genetics, Bioinformatics and Computational Biology Graduate ProgramVirginia TechBlacksburgUSA
  4. 4.Institute of General MicrobiologyChristian-Albrechts-UniversityKielGermany
  5. 5.Departments of Biochemistry and Biological SciencesVirginia TechBlacksburgUSA
  6. 6.Laboratoire de Biologie Moléculaire et CellulaireNeuchâtelSwitzerland
  7. 7.Department of Plant and Microbial Biology, Koshland HallUniversity of CaliforniaBerkeleyUSA

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