Skip to main content
Log in

Efficiency of hydrogen photoproduction by photosystem I-enriched subchloroplast vesicles combined with Proteus mirabilis cells. Effects of some exogenous electron donors

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

High rates of hydrogen photoproduction are obtained when glutaraldehyde-fixed Photosystem I-enriched vesicles (Photosystem II-depleted) are added to hydrogenase-containing cells of Proteus mirabilis in the presence of the mediator methylviologen and a suitable electron donating system. This donor system includes ascorbate, dithioerythritol (DTE) and the mediator tetramethylphenylene-diamine (TMPD) and reduces the photosynthetic electron transfer chain at the level of plastocyanin. Both DTE and ascorbate are required for hydrogen photoproduction, DTE being the ultimate electron donor and ascorbate only having a catalytic function. Whereas the aerobic photoreduction of methylviologen is similar in the presence of DTE, ascorbate or both, under anaerobic conditions only combination of both compounds results in a high and stable amount of reduced methylviologen that can be utilized by the hydrogenase. It is concluded that oxidation reactions of reduced methylviologen, competing with the hydrogenase, rather than methylviologen photoreduction, limit hydrogen photoproduction in the presence of either DTE or ascorbate. These oxidation reactions are suggested to involve back reactions to the oxidized form(s) of ascorbate and DTE but backflow to the photosynthetic electron transfer chain (i.e. cyclic electron transfer) can not be excluded.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Tes:

N-tris (hydroxymethyl) methyl-2-aminoethanesulfonic acid

DTE:

1,4-dithioerythritol

TMPD, N,N,N′:

N′-tetramethyl-p-phenylenediamine

DCMU:

3-(3′, 4′-dichlorophenyl)-1, 1,-dimethylureum

EDAC:

1-ethyl-3-(3-dimethylaminopropyl)-carbodiimide

DNP-INT:

2-iodo-6-isopropyl-3-methyl-2′, 4, 4′-trinitrodiphenyl ether

DBMIB:

2,5-dibromo-3-methyl-6-isopropyl-benzoquinone

PS:

photosystem

Chl:

chlorophyll

References

  1. Adams MWW, Mortenson LE and Chen J-S (1981) Hydrogenase. Biochim Biophys Acta 594: 105–176

    Google Scholar 

  2. Arnon DI, Mitsui A and Paneque A (1961) Photoproduction of hydrogen gas coupled with photosynthetic phosphorylation. Science 134: 1425

    Google Scholar 

  3. Ben-Amotz A and Gibbs M (1975) H2 metabolism in photosynthetic organism. Light-dependent H2 evolution by preparation from Chlamydomonas, Scenedesmus and spinach. Biochem Biophys Res Commun 61, 355–359

    Google Scholar 

  4. Benemann JR, Berenson JA, Kaplan NS and Kamer MD (1973) Hydrogen evolution by chloroplast-ferredoxin-hydrogenase system. Proc Natl Acad Sci USA 70: 2317–2320

    Google Scholar 

  5. Bernstein JD and Olson JM (1981) Photoreduction of hydrogen by membranes of green photosynthetic bacteria. In Akoyunoglou G, ed. Photosynthesis Vl. pp. 675–680. Philadelphia: Balaban International Science Services

    Google Scholar 

  6. Bruinsma J (1961) A comment on the spectrophotometric determination of chlorophyll. Biochim Biophys Acta 52: 576–578

    Google Scholar 

  7. Cleland WW (1964) Dithiothreitol, a new projective reagent for SH groups. Biochemistry 3: 480–482

    Google Scholar 

  8. Cuendet P and Gratzel M (1981) Photoproduction of H2 from isolated chloroplasts through ultrafine Pt catalysts and different viologen relays. Photobiochem Photobiophys 2:93–103

    Google Scholar 

  9. Fry I, Papageorgiu G, Tel-Or E and Packer L (1977) Reconstitution of a system for H2 evolution with chloroplasts, ferredoxin and hydrogenase. Z Naturforsch 32c: 110–117

    Google Scholar 

  10. Gisby PE and Hall DO (1981) Biophotolytic hydrogen production using alginate immobilized chloroplasts, enzymes and synthetic catalysts. In Akoyunoglou G, ed. Photosynthesis VI, pp. 655–664, Philadelphia: Balaban International Science Services

    Google Scholar 

  11. Hauska GA, McCarty RE and Racker E (1970) The site of phosphorylation associated with Photosystem I. Biochim Biophys Acta 197: 206–218

    Google Scholar 

  12. Hauska GA, Reimer S and Trebst A (1974) Native and artificial energy-conserving sites in cyclic photophosphorylation systems. Biochim Biophys Acta 357:1–13

    Google Scholar 

  13. Hoffmann D, Thauer R and Trebst A (1977) Photosynthetic hydrogen evolution by spinach chloroplasts coupled to a Clostridium hydrogenase. Z Naturforsch 32c: 357–362

    Google Scholar 

  14. Izawa S, Kraayenhof R, Ruuge EK and Devault D (1973) The site of KCN inhibition in the photosynthetic electron transport pathway. Biochim Biophys Acta 314: 328–339

    Google Scholar 

  15. Karube L, Matsunaga T, Otsuka T, Kayano H and Suzuki S (1981) Hydrogen evolution by co-immobilized chloroplasts and Clostridium butyricum. Biochim Biophys Acta 637:490–495

    Google Scholar 

  16. Kraayenhof R, Schuurmans JJ, Valkier LJ, Veen JPC, Van Marum D and Jasper CGG (1982) A thermoelectrically regulated multipurpose cuvette for simultaneous time-dependent measurements. Anal Biochem 127, 93–99

    Google Scholar 

  17. Krab K, Boog R and Peters FALJ (1984) Biophotolysis: generation of lowpotential reducing equivalents by Photosystem I-enriched subchloroplast vesicles. In Sybesma C, ed. Photosynthesis, in press. Brussel

  18. Krab K, Oltmann LF and Stouthamer AH (1982) Linkage of formate hydrogenlyase with anaerobic respiration in Proteus mirabilis. Biochim Biophys Acta 679:51–59

    Google Scholar 

  19. Krasnovsky AA, Van Ni C, Nikandrov VV and Brin GP (1980) Efficiency of hydrogen photoproduction by chloroplast-bacterial hydrogenase systems. Plant Physiol 66:925–930

    Google Scholar 

  20. Law MY, Charles SA and Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacea oleracea) chloroplasts. Biochem J 210:899–903

    Google Scholar 

  21. Lowry OH, Rosebrough NJ, Farr AL and Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Google Scholar 

  22. McCarty RE (1974) Inhibition of electron transport in chloroplasts between the two photosystems by a water-soluble carbodiimide. Arch Biochem Biophys 161: 93–99

    Google Scholar 

  23. Muallem A and Hall DO (1982) Ascorbate as a substrate for photoproduction of hydrogen by Photosystem I of chloroplasts. Plant Physiol 69:1116–1120

    Google Scholar 

  24. Packer L and Cullingford W (1978) Stoichiometry of H2 production by an in vitro chloroplast, ferredoxin, hydrogenase reconstituted system. Z Naturforsch 33c: 113–115

    Google Scholar 

  25. Peters FALJ, Van Wielink JE, Wong Fong Sang HW, De Vries S and Kraayenhof R (1983) Studies on well-coupled Photosystem I-enriched subchloroplast vesicles. Content and redox properties of electron transfer components. Biochim Biophys Acta 722, 460–470

    Google Scholar 

  26. Rao KK, Rosa L and Hall DO (1976) Prolonged production of hydrogen gas by a chloroplast biocatalytic system. Biochem Biophys Res Commun 68:21–28

    Google Scholar 

  27. Rosen MM and Krasna AI (1980) Limiting reactions in hydrogen photoreduction by chloroplasts and hydrogenase. Photochem Photobiol 31:259–265

    Google Scholar 

  28. Trebst A (1980) Inhibitors in electron flow: tools for the functional and structural localization of carriers and energy conservation sites. Meth Enzymol 69: 675–715

    Google Scholar 

  29. Wang R, Healy FP and Myers J (1971) Amperometric measurement of hydrogen evolution in Chladynomonas. Plant Physiol 48:108–110

    Google Scholar 

  30. West J and Packer L (1970) The effect of glutaraldehyde on light-induced H+ changes, electron transport and phosphorylation in pea chloroplasts. J Bioenerget 1, 405–412

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peters, F.A.L.J., Boog, R., Krab, K. et al. Efficiency of hydrogen photoproduction by photosystem I-enriched subchloroplast vesicles combined with Proteus mirabilis cells. Effects of some exogenous electron donors. Photosynth Res 5, 335–346 (1984). https://doi.org/10.1007/BF00034978

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00034978

Key words

Navigation