1887

Abstract

In , carotenoids are essential constituents of the photosynthetic apparatus and are assumed to prevent the formation of singlet oxygen by quenching of triplet bacteriochlorophyll (BChl ) . It was shown that small amounts of singlet oxygen are generated by incubation of under high light conditions. However, growth and survival rates were not affected. Higher amounts of singlet oxygen were generated by BChl in a carotenoid-deficient strain and led to a decrease in growth and survival rates. The data support earlier results on the pivotal role of carotenoids in the defence against stress caused by singlet oxygen. Results obtained under photo-oxidative stress conditions with strains impaired in carotenoid synthesis suggest that sphaeroidene and neurosporene provide less protection against methylene-blue-generated singlet oxygen than sphaeroidenone . Despite their protective function against singlet oxygen, relative amounts of carotenoids did not accumulate in wild-type cultures under photo-oxidative stress, and relative mRNA levels of phytoene dehydrogenase and sphaeroidene monooxygenase did not increase. In contrast, singlet oxygen specifically induced the expression of glutathione peroxidase and a putative Zn-dependent hydrolase, but mRNA levels of hydrogen-peroxide-degrading catalase E were not significantly affected by photo-oxidative stress. Based on these results, it is suggested that singlet oxygen acts as a specific signal for gene expression in . Presumably transcriptional regulators exist to specifically induce the expression of genes involved in the response to stress caused by singlet oxygen.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27789-0
2005-06-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/6/mic1511927.html?itemId=/content/journal/micro/10.1099/mic.0.27789-0&mimeType=html&fmt=ahah

References

  1. Bauer C. E., Elsen S., Bird T. H. 1999; Mechanisms for redox control of gene expression. Annu Rev Microbiol 53:495–523 [CrossRef]
    [Google Scholar]
  2. Borland C. F., McGarvey D. J., Truscott T. G., Cogdell R. J., Land E. J. 1987; Photophysical studies of bacteriochlorophyll a and bacteriopheophytin a singlet oxygen generation. J Photochem Photobiol B Biol 1:93–101 [CrossRef]
    [Google Scholar]
  3. Borland C. F., Cogdell R. J., Land E. J., Truscott T. G. 1989; Bacteriochlorophyll a triplet state and its interactions with bacterial carotenoids and oxygen. J Photochem Photobiol B Biol 3:227–245
    [Google Scholar]
  4. Briviba K., Klotz L. O., Sies H. 1997; Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol Chem 378:1259–1265
    [Google Scholar]
  5. Clayton R. K. 1966; Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo . Photochem Photobiol 5:669–677 [CrossRef]
    [Google Scholar]
  6. Cogdell R. J., Frank H. A. 1987; How carotenoids function in photosynthetic bacteria. Biochim Biophys Acta 895:63–79 [CrossRef]
    [Google Scholar]
  7. Cogdell R. J., Isaacs N. W., Howard T. D., McLuskey K., Fraser N. J., Prince S. M. 1999; How photosynthetic bacteria harvest solar energy. J Bacteriol 181:3869–3879
    [Google Scholar]
  8. Cogdell R. J., Howard T. D., Bittl R., Schlodder E., Geisenheimer I., Lubitz W. 2000; How carotenoids protect bacterial photosynthesis. Philos Trans R Soc Lond B Biol Sci 355:1345–1349 [CrossRef]
    [Google Scholar]
  9. Demmig-Adams B., Adams W. W., Ebbert V., Logan B. A. 1999; Ecophysiology of the Xanthophyll Cycle. In The Photochemistry of Carotenoids Edited by Frank H. A., Young A., Britton G., Cogdell R. J. Dordrecht: Kluwer;
    [Google Scholar]
  10. Di-Mascio P., Kaiser S., Sies H. 1989; Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys 274:532–538 [CrossRef]
    [Google Scholar]
  11. Drews G. 1983 Mikrobiologisches Praktikum Heidelberg: Springer;
    [Google Scholar]
  12. Edge R., Truscott T. G. 1999; Carotenoid radicals and the interaction of carotenoids with active oxygen species. In The Photochemistry of Carotenoids pp 223–234 Edited by Frank H. A., Young A. J., Britton G., Cogdell R. J. Dordrecht: Kluwer;
    [Google Scholar]
  13. Epe B. 1991; Genotoxicity of singlet oxygen. Chem Biol Interact 80:239–260 [CrossRef]
    [Google Scholar]
  14. Fiedor J., Fiedor L., Winkler J., Scherz A., Scheer H. 2001; Photodynamics of the bacteriochlorophyll-carotenoid system. 1. Bacteriochlorophyll-photosensitized oxygenation of beta-carotene in acetone. Photochem Photobiol 74:64–71 [CrossRef]
    [Google Scholar]
  15. Fiedor J., Fiedor L., Kammhuber N., Scherz A., Scheer H. 2002; Photodynamics of the bacteriochlorophyll-carotenoid system. 2. Influence of central metal, solvent and beta-carotene on photobleaching of bacteriochlorophyll derivatives. Photochem Photobiol 76:145–152 [CrossRef]
    [Google Scholar]
  16. Foote C. S. 1976; Photosensitised oxidation and singlet oxygen: consequences in biological systems. In Free Radicals and Biological Systems pp 85–133 Edited by Pryor W. A. New York: Academic Press;
    [Google Scholar]
  17. Foote C. S., Clennan E. L. 1995; Properties and reactions of singlet oxygen. In Active Oxygen in Chemistry pp 105–141 Edited by Foote C. S., Valentine J. S., Greenberg A., Liebmann J. F. London: Blackie Academic and Professional;
    [Google Scholar]
  18. Foote C. S., Denny R. W. 1968; Chemistry of singlet oxygen. VII. Quenching by β-carotene. J Am Chem Soc 90:6233–6235 [CrossRef]
    [Google Scholar]
  19. Foote C. S., Chang Y. C., Denny R. W. 1970; Chemistry of singlet oxygen. X. Carotenoid quenching parallels biological protection. J Am Chem Soc 92:5216–5218 [CrossRef]
    [Google Scholar]
  20. Foyer C. H., Jeremy H. 1999; Relationships between antioxidant metabolism and carotenoids in the regulation of photosynthesis. In The Photochemistry of Carotenoids Edited by Frank H. A., Young A. J., Britton G., Cogdell R. J. Dordrecht: Kluwer;
    [Google Scholar]
  21. Fraser N. J., Hashimoto H., Cogdell R. J. 2001; Carotenoids and bacterial photosynthesis: the story so far. Photosynth Res 70:249–256 [CrossRef]
    [Google Scholar]
  22. Gorman A. A., Rodgers M. A. 1992; Current perspectives of singlet oxygen detection in biological environments. J Photochem Photobiol B Biol 14:159–176 [CrossRef]
    [Google Scholar]
  23. Gregor J., Klug G. 1999; Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol Lett 179:1–9 [CrossRef]
    [Google Scholar]
  24. Gregor J., Klug G. 2002; Oxygen-regulated expression of genes for pigment binding proteins in Rhodobacter capsulatus . J Mol Microbiol Biotechnol 4:249–253
    [Google Scholar]
  25. Griffiths M., Sistrom W. R., Cohen-Bazire G., Stanier R. Y. 1955; Function of carotenoids in photosynthesis. Nature 176:1211–1214 [CrossRef]
    [Google Scholar]
  26. Hideg É., Kálai T., Hideg K., Vass I. 2000; Do oxidative stress conditions impairing photosynthesis in the light manifest as photoinhibition?. Philos Trans R Soc Lond B Biol Sci 355:1511–1516 [CrossRef]
    [Google Scholar]
  27. Hirayama O., Nakamura K., Hamada S., Kobayasi Y. 1994; Singlet oxygen quenching ability of naturally occurring carotenoids. Lipids 29:149–150 [CrossRef]
    [Google Scholar]
  28. Hodgson D. A., Murillo F. J. 1993; Genetics of regulation and pathway of synthesis of carotenoids. In Myxobacteria II pp 157–181 Edited by Dworkin M., Kaiser D. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  29. Imhoff J. F., Pfennig N, Trüper H. G. 1984; Rearrangements of the species and genera of the phototrophic purple nonsulfur bacteria. Int J Syst Bacteriol 34:340–343 [CrossRef]
    [Google Scholar]
  30. Kálai T., Hideg É., Vass I., Hideg K. 1998; Double (fluorescent and spin) sensors for detection of reactive oxygen species in the thylakoid membrane. Free Rad Biol Med 24:649–652 [CrossRef]
    [Google Scholar]
  31. Kochevar I. E. 2004; Singlet oxygen signaling: from intimate to global. In Science's STKE [Electronic Resource] Signal Transduction Knowledge Environmentpe7 doi: 10.1126/stke.2212004pe7
    [Google Scholar]
  32. Kochevar I. E., Redmond R. W. 2000; Photosensitized production of singlet oxygen. In Methods of Enzymology: Singlet Oxygen, UV-A and Ozone pp 20–28 Edited by Packer L., Sies H. London: Academic Press;
    [Google Scholar]
  33. Krieger-Liszkay A. 2004; Singlet oxygen production in photosynthesis. J Exp Bot1–10
    [Google Scholar]
  34. Krinsky N. I. 1978; Non-photosynthetic functions of carotenoids. Philos Trans R Soc Lond B Biol Sci 284:581–590 [CrossRef]
    [Google Scholar]
  35. Lang H. P., Hunter C. N. 1994; The relationship between carotenoid biosynthesis and the assembly of the light-harvesting LH2 complex in Rhodobacter sphaeroides . Biochem J 298:197–205
    [Google Scholar]
  36. Lang H. P., Cogdell R. J., Gardiner A. T., Hunter C. N. 1994; Early steps in carotenoid biosynthesis: sequences and transcriptional analysis of the crtI and crtB genes of Rhodobacter sphaeroides and overexpression and reactivation of crtI in Escherichia coli and R. sphaeroides . J Bacteriol 176:3859–3869
    [Google Scholar]
  37. Lang H. P., Cogdell R. J., Takaichi S., Hunter C. N. 1995; Complete DNA sequence, specific Tn5 insertion map, and gene assignment of the carotenoid biosynthesis pathway ofRhodobacter sphaeroides . J Bacteriol 177:2064–2073
    [Google Scholar]
  38. Leisinger U., Rufenacht K., Fischer B., Pesaro M., Spengler A., Zehnder A. J., Eggen R. I. 2001; The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol Biol 46:395–408 [CrossRef]
    [Google Scholar]
  39. Li K., Hartig E., Klug G. 2003a; Thioredoxin 2 is involved in oxidative stress defence and redox-dependent expression of photosynthesis genes in Rhodobacter capsulatus. Microbiology 149:419–430 [CrossRef]
    [Google Scholar]
  40. Li K., Pasternak C., Klug G. 2003b; Expression of the trxA gene for thioredoxin 1 in Rhodobacter sphaeroides during oxidative stress. Arch Microbiol 180:484–489 [CrossRef]
    [Google Scholar]
  41. Li K., Hein S., Zou W., Klug G. 2004; The glutathione-glutaredoxin system in Rhodobacter capsulatus: part of a complex regulatory network controlling defense against oxidative stress. J Bacteriol 186:6800–6808 [CrossRef]
    [Google Scholar]
  42. Limantara L., Fujii R., Zhang J. P., Kakuno T., Hara H., Kawamori A., Yagura T., Cogdell R. J., Koyama Y. 1998; Generation of triplet and cation-radical bacteriochlorophyll a in carotenoidless LH1 and LH2 antenna complexes from Rhodobacter sphaeroides . Biochemistry 37:17469–17486 [CrossRef]
    [Google Scholar]
  43. Morgan P. E., Dean R. T., Davies M. J. 2004; Protective mechanisms against peptide and protein peroxides generated by singlet oxygen. Free Rad Biol Med 36:484–496 [CrossRef]
    [Google Scholar]
  44. O'Gara J. P., Kaplan S. 1997; Evidence for the role of redox carriers in photosynthesis gene expression and carotenoid biosynthesis in Rhodobacter sphaeroides 2.4.1. J Bacteriol 179:1951–1961
    [Google Scholar]
  45. op-den-Camp R. G., Przybyla D., Ochsenbein C. 9 other authors 2003; Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis . Plant Cell 15:2320–2332 [CrossRef]
    [Google Scholar]
  46. Ouchane S., Picaud M., Vernotte C., Astier C. 1997; Photooxidative stress stimulates illegitimate recombination and mutability in carotenoid-less mutants of Rubrivivax gelatinosus. EMBO J 16:4777–4787 [CrossRef]
    [Google Scholar]
  47. Pappas C. T., Sram J., Moskvin O. V. & 7 other authors; 2004; Construction and validation of the Rhodobacter sphaeroides 2.4.1 DNA microarray: transcriptome flexibility at diverse growth modes. J Bacteriol 186:4748–4758 [CrossRef]
    [Google Scholar]
  48. Paul A., Hackbarth S., Vogt R. D., Roder B., Burnison B. K., Steinberg C. E. 2004; Photogeneration of singlet oxygen by humic substances: comparison of humic substances of aquatic and terrestrial origin. Photochem Photobiol Sci 3:273–280 [CrossRef]
    [Google Scholar]
  49. Permentier H. P., Neerken S., Overmann J., Amesz J. 2001; A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm. Biochemistry 40:5573–5578 [CrossRef]
    [Google Scholar]
  50. Pfaffl M. W. 2001; A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45 [CrossRef]
    [Google Scholar]
  51. Schroeder W. A., Johnson E. A. 1995; Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Pfaffia rhodozyma . J Biol Chem 270:18374–18379 [CrossRef]
    [Google Scholar]
  52. Sies H., Menck C. F. 1992; Singlet oxygen induced DNA damage. Mutat Res 275:367–375 [CrossRef]
    [Google Scholar]
  53. Takaichi S. 1999; Carotenoids and carotenogenesis in anoxygenic photosynthetic bacteria. In The Photochemistry of Carotenoids pp 39–69 Edited by Frank H. A., Young A., Britton G., Cogdell R. J. Dordrecht: Kluwer;
    [Google Scholar]
  54. Tandori J., Hideg E., Nagy L., Maroti P., Vass I. 2001; Photoinhibition of carotenoidless reaction centers from Rhodobacter sphaeroides by visible light. Effects on protein structure and electron transport. Photosynth Res 70:175–184 [CrossRef]
    [Google Scholar]
  55. Van Liere E., Walsby A. 1982; Interaction of cyanobacteria with light. In The Biology of Cyanobacteria pp 9–45 Edited by Carr N. G., Whitton B. A. Oxford: Blackwell;
    [Google Scholar]
  56. van Niel C. B. 1941; The culture, general physiology, morphology, and classification of the non-sulfur purple and brown bacteria. Bacteriol Rev 8:1–118
    [Google Scholar]
  57. Wagner D., Przybyla D., op-den-Camp R. G. 8 other authors 2004; The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185 [CrossRef]
    [Google Scholar]
  58. Yeliseev A. A., Kaplan S. 1997; Anaerobic carotenoid biosynthesis in Rhodobacter sphaeroides 2.4.1: H2O is a source of oxygen for the 1-methoxy group of spheroidene but not for the 2-oxo group of spheroidenone. FEBS Lett 403:10–14 [CrossRef]
    [Google Scholar]
  59. Zeilstra-Ryalls J. H., Kaplan S. 2004; Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm. Cell Mol Life Sci 61:417–436 [CrossRef]
    [Google Scholar]
  60. Zeller T., Klug G. 2004; Detoxification of hydrogen peroxide and expression of catalase genes in Rhodobacter. Microbiology 150:3451–3462 [CrossRef]
    [Google Scholar]
  61. Züllig H. 1985; Pigmente phototropher bakterien in seesedimenten und ihre bedeutung für die seenforschung. Schweiz Ztg Hydrol 47:87–126 [CrossRef]
    [Google Scholar]
  62. Zurdo J., Fernandez-Cabrera C., Ramirez J. M. 1993; A structural role of the carotenoid in the light-harvesting II protein of Rhodobacter capsulatus. Biochem J 290:531–537
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27789-0
Loading
/content/journal/micro/10.1099/mic.0.27789-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error