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. 1995 May 1;14(9):1845–1853. doi: 10.1002/j.1460-2075.1995.tb07176.x

Molecular identification of an ABC transporter complex for manganese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process.

V V Bartsevich 1, H B Pakrasi 1
PMCID: PMC398283  PMID: 7743991

Abstract

During photosynthesis, the photosystem II (PSII) pigment-protein complex catalyzes oxygen evolution, a reaction in which a four-manganese ensemble plays a crucial role. Using a newly developed selection scheme, we have isolated BP13, a random photosynthesis-deficient mutant strain of the cyanobacterium, Synechocystis 6803. This mutant grew slowly under photoautotrophic conditions, and had a low oxygen evolution activity. Biochemical analysis revealed that the lesion in this mutant strain had specifically affected the Mn ensemble in PSII. Interestingly, incubation of BP13 cells with micromolar levels of added Mn induced rapid recovery of oxygen evolution activity. The mutant could be complemented with a fragment of wild-type chromosomal DNA containing three closely linked genes, mntA, mntB and mntC. These gene products showed significant sequence similarities with polypeptide components of bacterial permeases that are members of the 'ABC (ATP binding cassette) superfamily' of transporter proteins. We determined that in the BP13 strain, a single nucleotide change had resulted in the replacement of an alanine by an aspartic acid residue in MntA, a soluble protein containing ATP binding motifs. These results suggest that the mntCAB gene cluster encodes polypeptide components of a Mn transporter, the first such protein complex identified in any organism.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Anbudurai P. R., Mor T. S., Ohad I., Shestakov S. V., Pakrasi H. B. The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem II reaction center complex. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8082–8086. doi: 10.1073/pnas.91.17.8082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anbudurai P. R., Pakrasi H. B. Mutational analysis of the PsbL protein of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Z Naturforsch C. 1993 Mar-Apr;48(3-4):267–274. doi: 10.1515/znc-1993-3-424. [DOI] [PubMed] [Google Scholar]
  4. Andersen R. N., Ganeshkumar N., Kolenbrander P. E. Cloning of the Streptococcus gordonii PK488 gene, encoding an adhesin which mediates coaggregation with Actinomyces naeslundii PK606. Infect Immun. 1993 Mar;61(3):981–987. doi: 10.1128/iai.61.3.981-987.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Astier C., Elmorjani K., Meyer I., Joset F., Herdman M. Photosynthetic mutants of the cyanobacteria Synechocystis sp. strains PCC 6714 and PCC 6803: sodium p-hydroxymercuribenzoate as a selective agent. J Bacteriol. 1984 May;158(2):659–664. doi: 10.1128/jb.158.2.659-664.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cheniae G. M., Martin I. F. Photoreaction of manganese catalyst in photosynthetic oxygen evolution. Plant Physiol. 1969 Mar;44(3):351–360. doi: 10.1104/pp.44.3.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Debus R. J. The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta. 1992 Oct 16;1102(3):269–352. doi: 10.1016/0005-2728(92)90133-m. [DOI] [PubMed] [Google Scholar]
  8. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dzelzkalns V. A., Bogorad L. Molecular analysis of a mutant defective in photosynthetic oxygen evolution and isolation of a complementing clone by a novel screening procedure. EMBO J. 1988 Feb;7(2):333–338. doi: 10.1002/j.1460-2075.1988.tb02817.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fath M. J., Kolter R. ABC transporters: bacterial exporters. Microbiol Rev. 1993 Dec;57(4):995–1017. doi: 10.1128/mr.57.4.995-1017.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fenno J. C., LeBlanc D. J., Fives-Taylor P. Nucleotide sequence analysis of a type 1 fimbrial gene of Streptococcus sanguis FW213. Infect Immun. 1989 Nov;57(11):3527–3533. doi: 10.1128/iai.57.11.3527-3533.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ganeshkumar N., Hannam P. M., Kolenbrander P. E., McBride B. C. Nucleotide sequence of a gene coding for a saliva-binding protein (SsaB) from Streptococcus sanguis 12 and possible role of the protein in coaggregation with actinomyces. Infect Immun. 1991 Mar;59(3):1093–1099. doi: 10.1128/iai.59.3.1093-1099.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Green L. S., Laudenbach D. E., Grossman A. R. A region of a cyanobacterial genome required for sulfate transport. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1949–1953. doi: 10.1073/pnas.86.6.1949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Higgins C. F. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. doi: 10.1146/annurev.cb.08.110192.000435. [DOI] [PubMed] [Google Scholar]
  15. Hyde S. C., Emsley P., Hartshorn M. J., Mimmack M. M., Gileadi U., Pearce S. R., Gallagher M. P., Gill D. R., Hubbard R. E., Higgins C. F. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature. 1990 Jul 26;346(6282):362–365. doi: 10.1038/346362a0. [DOI] [PubMed] [Google Scholar]
  16. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  17. Mannan R. M., Pakrasi H. B. Dark heterotrophic growth conditions result in an increase in the content of photosystem II units in the filamentous cyanobacterium Anabaena variabilis ATCC 29413. Plant Physiol. 1993 Nov;103(3):971–977. doi: 10.1104/pp.103.3.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Omata T., Andriesse X., Hirano A. Identification and characterization of a gene cluster involved in nitrate transport in the cyanobacterium Synechococcus sp. PCC7942. Mol Gen Genet. 1993 Jan;236(2-3):193–202. doi: 10.1007/BF00277112. [DOI] [PubMed] [Google Scholar]
  19. Pakrasi H. B., Williams J. G., Arntzen C. J. Targeted mutagenesis of the psbE and psbF genes blocks photosynthetic electron transport: evidence for a functional role of cytochrome b559 in photosystem II. EMBO J. 1988 Feb;7(2):325–332. doi: 10.1002/j.1460-2075.1988.tb02816.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rhiel E., Stirewalt V. L., Gasparich G. E., Bryant D. A. The psaC genes of Synechococcus sp. PCC7002 and Cyanophora paradoxa: cloning and sequence analysis. Gene. 1992 Mar 1;112(1):123–128. doi: 10.1016/0378-1119(92)90313-e. [DOI] [PubMed] [Google Scholar]
  21. Saurin W., Dassa E. Sequence relationships between integral inner membrane proteins of binding protein-dependent transport systems: evolution by recurrent gene duplications. Protein Sci. 1994 Feb;3(2):325–344. doi: 10.1002/pro.5560030216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Saurin W., Köster W., Dassa E. Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins. Mol Microbiol. 1994 Jun;12(6):993–1004. doi: 10.1111/j.1365-2958.1994.tb01087.x. [DOI] [PubMed] [Google Scholar]
  23. Shestakov S. V., Anbudurai P. R., Stanbekova G. E., Gadzhiev A., Lind L. K., Pakrasi H. B. Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing protease. Analysis of a spontaneous photosystem II-deficient mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem. 1994 Jul 29;269(30):19354–19359. [PubMed] [Google Scholar]
  24. Shukla V. K., Stanbekova G. E., Shestakov S. V., Pakrasi H. B. The D1 protein of the photosystem II reaction-centre complex accumulates in the absence of D2: analysis of a mutant of the cyanobacterium Synechocystis sp. PCC 6803 lacking cytochrome b559. Mol Microbiol. 1992 Apr;6(7):947–956. doi: 10.1111/j.1365-2958.1992.tb01544.x. [DOI] [PubMed] [Google Scholar]
  25. Silver S., Walderhaug M. Gene regulation of plasmid- and chromosome-determined inorganic ion transport in bacteria. Microbiol Rev. 1992 Mar;56(1):195–228. doi: 10.1128/mr.56.1.195-228.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Staudenmaier H., Van Hove B., Yaraghi Z., Braun V. Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron(III) dicitrate in Escherichia coli. J Bacteriol. 1989 May;171(5):2626–2633. doi: 10.1128/jb.171.5.2626-2633.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tam R., Saier M. H., Jr Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev. 1993 Jun;57(2):320–346. doi: 10.1128/mr.57.2.320-346.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vermaas W., Charité J., Shen G. Z. Glu-69 of the D2 protein in photosystem II is a potential ligand to Mn involved in photosynthetic oxygen evolution. Biochemistry. 1990 Jun 5;29(22):5325–5332. doi: 10.1021/bi00474a017. [DOI] [PubMed] [Google Scholar]
  29. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [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. von Heijne G. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol. 1992 May 20;225(2):487–494. doi: 10.1016/0022-2836(92)90934-c. [DOI] [PubMed] [Google Scholar]

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