Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Aug 1;90(15):7134–7138. doi: 10.1073/pnas.90.15.7134

Early evolution of photosynthesis: clues from nitrogenase and chlorophyll iron proteins.

D H Burke 1, J E Hearst 1, A Sidow 1
PMCID: PMC47090  PMID: 8346226

Abstract

Chlorophyll (Chl) is often viewed as having preceded bacteriochlorophyll (BChl) as the primary photoreceptor pigment in early photosynthetic systems because synthesis of Chl requires one fewer enzymatic reduction than does synthesis of BChl. We have conducted statistical DNA sequence analyses of the two reductases involved in Chl and BChl synthesis, protochlorophyllide reductase and chlorin reductase. Both are three-subunit enzymes in which each subunit from one reductase shares significant amino acid identity with a subunit of the other, indicating that the two enzymes are derived from a common three-subunit ancestral reductase. The "chlorophyll iron protein" subunits, encoded by the bchL and bchX genes in the purple bacterium Rhodobacter capsulatus, also share amino acid sequence identity with the nitrogenase iron protein, encoded by nifH. When nitrogenase iron proteins are used as outgroups, the chlorophyll iron protein tree is rooted on the chlorine reductase lineage. This rooting suggests that the last common ancestor of all extant photosynthetic eubacteria contained BChl, not Chl, in its reaction center, and implies that Chl-containing reaction centers were a late invention unique to the cyanobacteria/chloroplast lineage.

Full text

PDF
7134

Images in this article

7136Fig. 3
on p.7136

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blankenship R. E. Origin and early evolution of photosynthesis. Photosynth Res. 1992;33:91–111. [PubMed] [Google Scholar]
  2. Bowie J. U., Lüthy R., Eisenberg D. A method to identify protein sequences that fold into a known three-dimensional structure. Science. 1991 Jul 12;253(5016):164–170. doi: 10.1126/science.1853201. [DOI] [PubMed] [Google Scholar]
  3. Burke D. H., Alberti M., Hearst J. E. The Rhodobacter capsulatus chlorin reductase-encoding locus, bchA, consists of three genes, bchX, bchY, and bchZ. J Bacteriol. 1993 Apr;175(8):2407–2413. doi: 10.1128/jb.175.8.2407-2413.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke D. H., Alberti M., Hearst J. E. bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants. J Bacteriol. 1993 Apr;175(8):2414–2422. doi: 10.1128/jb.175.8.2414-2422.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Choquet Y., Rahire M., Girard-Bascou J., Erickson J., Rochaix J. D. A chloroplast gene is required for the light-independent accumulation of chlorophyll in Chlamydomonas reinhardtii. EMBO J. 1992 May;11(5):1697–1704. doi: 10.1002/j.1460-2075.1992.tb05220.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Deits T. L., Howard J. B. Effect of salts on Azotobacter vinelandii nitrogenase activities. Inhibition of iron chelation and substrate reduction. J Biol Chem. 1990 Mar 5;265(7):3859–3867. [PubMed] [Google Scholar]
  7. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. doi: 10.1007/BF01734359. [DOI] [PubMed] [Google Scholar]
  8. Fujita Y., Takahashi Y., Kohchi T., Ozeki H., Ohyama K., Matsubara H. Identification of a novel nifH-like (frxC) protein in chloroplasts of the liverwort Marchantia polymorpha. Plant Mol Biol. 1989 Nov;13(5):551–561. doi: 10.1007/BF00027315. [DOI] [PubMed] [Google Scholar]
  9. Georgiadis M. M., Komiya H., Chakrabarti P., Woo D., Kornuc J. J., Rees D. C. Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science. 1992 Sep 18;257(5077):1653–1659. doi: 10.1126/science.1529353. [DOI] [PubMed] [Google Scholar]
  10. Hasegawa M., Kishino H., Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22(2):160–174. doi: 10.1007/BF02101694. [DOI] [PubMed] [Google Scholar]
  11. Hearst J. E., Alberti M., Doolittle R. F. A putative nitrogenase reductase gene found in the nucleotide sequences from the photosynthetic gene cluster of R. capsulata. Cell. 1985 Jan;40(1):219–220. doi: 10.1016/0092-8674(85)90325-3. [DOI] [PubMed] [Google Scholar]
  12. Hein J. A new method that simultaneously aligns and reconstructs ancestral sequences for any number of homologous sequences, when the phylogeny is given. Mol Biol Evol. 1989 Nov;6(6):649–668. doi: 10.1093/oxfordjournals.molbev.a040577. [DOI] [PubMed] [Google Scholar]
  13. Howard J. B., Davis R., Moldenhauer B., Cash V. L., Dean D. Fe:S cluster ligands are the only cysteines required for nitrogenase Fe-protein activities. J Biol Chem. 1989 Jul 5;264(19):11270–11274. [PubMed] [Google Scholar]
  14. Højrup P., Gerola P., Hansen H. F., Mikkelsen J. M., Shahed A. E., Knudsen J., Roepstorff P., Olson J. M. The amino acid sequence of a major protein component in the light harvesting complex of the green photosynthetic bacterium Chlorobium limicola f. thiosulfatophilum. Biochim Biophys Acta. 1991 Apr 8;1077(2):220–224. doi: 10.1016/0167-4838(91)90061-4. [DOI] [PubMed] [Google Scholar]
  15. Kishino H., Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989 Aug;29(2):170–179. doi: 10.1007/BF02100115. [DOI] [PubMed] [Google Scholar]
  16. Mortenson L. E., Thorneley R. N. Structure and function of nitrogenase. Annu Rev Biochem. 1979;48:387–418. doi: 10.1146/annurev.bi.48.070179.002131. [DOI] [PubMed] [Google Scholar]
  17. Nitschke W., Rutherford A. W. Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci. 1991 Jul;16(7):241–245. doi: 10.1016/0968-0004(91)90095-d. [DOI] [PubMed] [Google Scholar]
  18. Normand P., Bousquet J. Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol. 1989 Nov;29(5):436–447. doi: 10.1007/BF02602914. [DOI] [PubMed] [Google Scholar]
  19. Normand P., Gouy M., Cournoyer B., Simonet P. Nucleotide sequence of nifD from Frankia alni strain ArI3: phylogenetic inferences. Mol Biol Evol. 1992 May;9(3):495–506. doi: 10.1093/oxfordjournals.molbev.a040737. [DOI] [PubMed] [Google Scholar]
  20. Ogura Y., Takemura M., Oda K., Yamato K., Ohta E., Fukuzawa H., Ohyama K. Cloning and nucleotide sequence of a frxC-ORF469 gene cluster of Synechocystis PCC6803: conservation with liverwort chloroplast frxC-ORF465 and nif operon. Biosci Biotechnol Biochem. 1992 May;56(5):788–793. doi: 10.1271/bbb.56.788. [DOI] [PubMed] [Google Scholar]
  21. Olson J. M., Pierson B. K. Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol. 1987;108:209–248. doi: 10.1016/s0074-7696(08)61439-4. [DOI] [PubMed] [Google Scholar]
  22. Orme-Johnson W. H. Molecular basis of biological nitrogen fixation. Annu Rev Biophys Biophys Chem. 1985;14:419–459. doi: 10.1146/annurev.bb.14.060185.002223. [DOI] [PubMed] [Google Scholar]
  23. Pau R. N. Nitrogenases without molybdenum. Trends Biochem Sci. 1989 May;14(5):183–186. doi: 10.1016/0968-0004(89)90271-5. [DOI] [PubMed] [Google Scholar]
  24. Pesole G., Bozzetti M. P., Lanave C., Preparata G., Saccone C. Glutamine synthetase gene evolution: a good molecular clock. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):522–526. doi: 10.1073/pnas.88.2.522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robson R. L. Identification of possible adenine nucleotide-binding sites in nitrogenase Fe- and MoFe-proteins by amino acid sequence comparison. FEBS Lett. 1984 Aug 6;173(2):394–398. doi: 10.1016/0014-5793(84)80812-1. [DOI] [PubMed] [Google Scholar]
  26. Souillard N., Magot M., Possot O., Sibold L. Nucleotide sequence of regions homologous to nifH (nitrogenase Fe protein) from the nitrogen-fixing archaebacteria Methanococcus thermolithotrophicus and Methanobacterium ivanovii: evolutionary implications. J Mol Evol. 1988;27(1):65–76. doi: 10.1007/BF02099731. [DOI] [PubMed] [Google Scholar]
  27. Souillard N., Sibold L. Primary structure, functional organization and expression of nitrogenase structural genes of the thermophilic archaebacterium Methanococcus thermolithotrophicus. Mol Microbiol. 1989 Apr;3(4):541–551. doi: 10.1111/j.1365-2958.1989.tb00200.x. [DOI] [PubMed] [Google Scholar]
  28. Suzuki J. Y., Bauer C. E. Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC). Plant Cell. 1992 Aug;4(8):929–940. doi: 10.1105/tpc.4.8.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Trost J. T., Brune D. C., Blankenship R. E. Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to Photosystem I. Photosynth Res. 1992;32:11–22. [PubMed] [Google Scholar]
  30. Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Willing A. H., Georgiadis M. M., Rees D. C., Howard J. B. Cross-linking of nitrogenase components. Structure and activity of the covalent complex. J Biol Chem. 1989 May 25;264(15):8499–8503. [PubMed] [Google Scholar]
  32. Willing A., Howard J. B. Cross-linking site in Azotobacter vinelandii complex. J Biol Chem. 1990 Apr 25;265(12):6596–6599. [PubMed] [Google Scholar]
  33. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wolle D., Kim C., Dean D., Howard J. B. Ionic interactions in the nitrogenase complex. Properties of Fe-protein containing substitutions for Arg-100. J Biol Chem. 1992 Feb 25;267(6):3667–3673. [PubMed] [Google Scholar]
  35. Yang Z. M., Bauer C. E. Rhodobacter capsulatus genes involved in early steps of the bacteriochlorophyll biosynthetic pathway. J Bacteriol. 1990 Sep;172(9):5001–5010. doi: 10.1128/jb.172.9.5001-5010.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES