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. 1996 Mar;8(3):539–553. doi: 10.1105/tpc.8.3.539

Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family.

R Rowan 1, S M Whitney 1, A Fowler 1, D Yellowlees 1
PMCID: PMC161119  PMID: 8721755

Abstract

Genes encoding ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) were cloned from dinoflagellate symbionts (Symbiodinium spp) of the giant clam Tridacna gigas and characterized. Strikingly, Symbiodinium Rubisco is completely different from other eukaryotic (form I) Rubiscos: it is a form II enzyme that is approximately 65% identical to Rubisco from Rhodospirillum rubrum (Rubisco forms I and II are approximately 25 to 30% identical); it is nuclear encoded by a multigene family; and the predominantly expressed Rubisco is encoded as a precursor polyprotein. One clone appears to contain a predominantly expressed Rubisco locus (rbcA), as determined by RNA gel blot analysis of Symbiodinium RNA and sequencing of purified Rubisco protein. Another contains an enigmatic locus (rbcG) that exhibits an unprecedented pattern of amino acid replacement but does not appear to be a pseudogene. The expression of rbcG has not been analyzed; it was detected only in the minor of two taxa of Symbiodinium that occur together in T. gigas. This study confirms and describes a previously unrecognized branch of Rubisco's evolution: a eukaryotic form II enzyme that participates in oxygenic photosynthesis and is encoded by a diverse, nuclear multigene family.

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Selected References

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  1. Andersen K., Caton J. Sequence analysis of the Alcaligenes eutrophus chromosomally encoded ribulose bisphosphate carboxylase large and small subunit genes and their gene products. J Bacteriol. 1987 Oct;169(10):4547–4558. doi: 10.1128/jb.169.10.4547-4558.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andrews T. J., Lorimer G. H., Tolbert N. E. Ribulose diphosphate oxygenase. I. Synthesis of phosphoglycolate by fraction-1 protein of leaves. Biochemistry. 1973 Jan 2;12(1):11–18. doi: 10.1021/bi00725a003. [DOI] [PubMed] [Google Scholar]
  3. Blank R. J., Trench R. K. Speciation and symbiotic dinoflagellates. Science. 1985 Aug 16;229(4714):656–658. doi: 10.1126/science.229.4714.656. [DOI] [PubMed] [Google Scholar]
  4. Brändén C. I., Lindqvist Y., Schneider G. Protein engineering of Rubisco. Acta Crystallogr B. 1991 Dec 1;47(Pt 6):824–835. doi: 10.1107/s0108768191007127. [DOI] [PubMed] [Google Scholar]
  5. Cavalier-Smith T. The number of symbiotic origins of organelles. Biosystems. 1992;28(1-3):91–108. doi: 10.1016/0303-2647(92)90011-m. [DOI] [PubMed] [Google Scholar]
  6. Hartman F. C., Harpel M. R. Structure, function, regulation, and assembly of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Annu Rev Biochem. 1994;63:197–234. doi: 10.1146/annurev.bi.63.070194.001213. [DOI] [PubMed] [Google Scholar]
  7. Houlné G., Schantz R. Characterization of cDNA sequences for LHCI apoproteins in Euglena gracilis: the mRNA encodes a large precursor containing several consecutive divergent polypeptides. Mol Gen Genet. 1988 Aug;213(2-3):479–486. doi: 10.1007/BF00339619. [DOI] [PubMed] [Google Scholar]
  8. Larimer F. W., Lee E. H., Mural R. J., Soper T. S., Hartman F. C. Intersubunit location of the active site of ribulose-bisphosphate carboxylase/oxygenase as determined by in vivo hybridization of site-directed mutants. J Biol Chem. 1987 Nov 15;262(32):15327–15329. [PubMed] [Google Scholar]
  9. Lorimer G. H., Badger M. R., Andrews T. J. The activation of ribulose-1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry. 1976 Feb 10;15(3):529–536. doi: 10.1021/bi00648a012. [DOI] [PubMed] [Google Scholar]
  10. Morden C. W., Delwiche C. F., Kuhsel M., Palmer J. D. Gene phylogenies and the endosymbiotic origin of plastids. Biosystems. 1992;28(1-3):75–90. doi: 10.1016/0303-2647(92)90010-v. [DOI] [PubMed] [Google Scholar]
  11. Palmer J. D. Comparative organization of chloroplast genomes. Annu Rev Genet. 1985;19:325–354. doi: 10.1146/annurev.ge.19.120185.001545. [DOI] [PubMed] [Google Scholar]
  12. Read B. A., Tabita F. R. High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial RubiSCO containing "algal" residue modifications. Arch Biochem Biophys. 1994 Jul;312(1):210–218. doi: 10.1006/abbi.1994.1301. [DOI] [PubMed] [Google Scholar]
  13. Reith M., Munholland J. A High-Resolution Gene Map of the Chloroplast Genome of the Red Alga Porphyra purpurea. Plant Cell. 1993 Apr;5(4):465–475. doi: 10.1105/tpc.5.4.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Rowan R., Powers D. A. A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science. 1991 Mar 15;251(4999):1348–1351. doi: 10.1126/science.251.4999.1348. [DOI] [PubMed] [Google Scholar]
  15. Schiff J. A., Schwartzbach S. D., Osafune T., Hase E. Photocontrol and processing of LHCP II apoprotein in Euglena: possible role of Golgi and other cytoplasmic sites. J Photochem Photobiol B. 1991 Nov;11(2):219–236. doi: 10.1016/1011-1344(91)80262-g. [DOI] [PubMed] [Google Scholar]
  16. Shashidhara L. S., Lim S. H., Shackleton J. B., Robinson C., Smith A. G. Protein targeting across the three membranes of the Euglena chloroplast envelope. J Biol Chem. 1992 Jun 25;267(18):12885–12891. [PubMed] [Google Scholar]
  17. Tessier L. H., Paulus F., Keller M., Vial C., Imbault P. Structure and expression of Euglena gracilis nuclear rbcS genes encoding the small subunits of the ribulose 1,5-bisphosphate carboxylase/oxygenase: a novel splicing process for unusual intervening sequences? J Mol Biol. 1995 Jan 6;245(1):22–33. doi: 10.1006/jmbi.1994.0003. [DOI] [PubMed] [Google Scholar]
  18. Whitney S. M., Shaw D. C., Yellowlees D. Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proc Biol Sci. 1995 Mar 22;259(1356):271–275. doi: 10.1098/rspb.1995.0040. [DOI] [PubMed] [Google Scholar]
  19. Yaguchi T., Chung S. Y., Igarashi Y., Kodama T. Cloning and sequence of the L2 form of RubisCO from a marine obligately autotrophic hydrogen-oxidizing bacterium, Hydrogenovibrio marinus strain MH-110. Biosci Biotechnol Biochem. 1994 Sep;58(9):1733–1737. doi: 10.1271/bbb.58.1733. [DOI] [PubMed] [Google Scholar]
  20. Zhang K. Y., Cascio D., Eisenberg D. Crystal structure of the unactivated ribulose 1,5-bisphosphate carboxylase/oxygenase complexed with a transition state analog, 2-carboxy-D-arabinitol 1,5-bisphosphate. Protein Sci. 1994 Jan;3(1):64–69. doi: 10.1002/pro.5560030109. [DOI] [PMC free article] [PubMed] [Google Scholar]

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