Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Bacterial responses to photo-oxidative stress

Nature Reviews Microbiology volume 7, pages 856–863 (2009)Cite this article

Key Points

  • Photo-oxidative stress is induced by the formation of the reactive oxygen species singlet oxygen, which is often caused by energy transfer from a light-excited donor to molecular oxygen.

  • Carotenoids protect photosynthetic organisms such as Rhodobacter sphaeroides from the photo-oxidative damage that is caused by this energy transfer.

  • The alternative σ-factor σE is the master regulator of the photo-oxidative stress response in R. sphaeroides.

  • Some known σE target genes are found in many bacteria (forming the core σE regulon), whereas others are predicted to be part of the photo-oxidative stress response in only a subset of species (known as the extended σE regulon).

  • The proposed core and extended σE regulons encode few proteins of known or predicted protective function, but how cells respond to photo-oxidative stress is largely unknown, as many target genes have no annotated function as yet.

  • Conservation of the proposed core σE regulon suggests that the photo-oxidative stress response is broadly represented both in photosynthetic bacteria and in non-photosynthetic microorganisms that can generate singlet oxygen from light-dependent or light-independent processes.

Abstract

Singlet oxygen is one of several reactive oxygen species that can destroy biomolecules, microorganisms and other cells. Traditionally, the response to singlet oxygen has been termed photo-oxidative stress, as light-dependent processes in photosynthetic cells are major biological sources of singlet oxygen. Recent work identifying a core set of singlet oxygen stress response genes across various bacterial species highlights the importance of this response for survival by both photosynthetic and non-photosynthetic cells. Here, we review how bacterial cells mount a transcriptional response to photo-oxidative stress in the context of what is known about bacterial stress responses to other reactive oxygen species.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Types of reactive oxygen species.
Figure 2: Sources of singlet oxygen.
Figure 3: Singlet oxygen activates a gene expression cascade in bacteria.
Figure 4: Natural history of the σE-dependent bacterial response to singlet oxygen.

Similar content being viewed by others

References

  1. Imlay, J. A. Pathways of oxidative damage. Annu. Rev. Microbiol. 57, 395–418 (2003).

    Article  CAS  PubMed  Google Scholar 

  2. Halliwell, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141, 312–322 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Storz, G. & Zheng, M. in Bacterial Stress Responses (eds Storz, G. & Hengge-Aronis, R.) 47–59 (ASM, Washington, 2000). Provides a comprehensive summary of bacterial responses to ROS created by type I reactions, with particular emphasis on the role of the oxyR and soxRS regulons.

    Google Scholar 

  4. Blankenship, R. E. & Hartman, H. The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23, 94–97 (1998).

    Article  CAS  PubMed  Google Scholar 

  5. Raymond, J., Zhaxybayeva, O., Gogarten, J. P. & Blankenship, R. E. Evolution of photosynthetic prokaryotes: a maximum-likelihood mapping approach. Phil. Trans. R. Soc. Lond. B Biol. Sci. 358, 223–230 (2003).

    Article  Google Scholar 

  6. Gennis, R. B. & Stewart, V. in Escherichia coli and Salmonella: Cellular and Molecular Biology (ed. Neidhardt, F. C.) 217–261 (ASM, Washington, 1999).

    Google Scholar 

  7. Briviba, K., Klotz, L.-O. & Sies, H. Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol. Chem. 378, 1259–1265 (1997). Summarizes how 1O 2 can be formed both in vivo and in vitro , the types of damage that it can inflict on molecules and cells and the types of cellular signalling events that it promotes.

    CAS  PubMed  Google Scholar 

  8. Sies, H. & Menck, C. F. M. Singlet oxygen induced DNA damage. Mutat. Res. 275, 367–375 (1992).

    Article  CAS  PubMed  Google Scholar 

  9. Epe, B., Pflaum, M. & Boiteux, S. DNA damage induced by photosensitizers in cellular and cell-free systems. Mutat. Res. 299, 135–145 (1993).

    Article  CAS  PubMed  Google Scholar 

  10. Davies, M. J. The oxidative environment and protein damage. Biochim. Biophys. Acta 1703, 93–109 (2005).

    Article  CAS  PubMed  Google Scholar 

  11. Borland, C. F., McGarvey, D. J., Truscott, T. G., Cogdell, R. J. & Land, E. J. Photophysical studies of bacteriochlorophyll a and bacteriopheophytin a – singlet oxygen generation. J. Photochem. Photobiol. B 1, 93–101 (1987).

    Article  CAS  Google Scholar 

  12. Cogdell, R. J. et al. How carotenoids protect bacterial photosynthesis. Phil. Trans. R. Soc. Lond. B 355, 1345–1349 (2000). Discusses structural studies of bacterial photosynthetic pigments in reaction centres and light-harvesting complexes combined with kinetic studies showing the decay of 3Bchl a * and the concomitant formation of triplet state carotenoids.

    Article  CAS  Google Scholar 

  13. Ryter, S. W. & Tyrrell, R. M. Singlet oxygen (1O2): a possible effector of eukaryotic gene expression. Free Radic. Biol. Med. 24, 1520–1534 (1998).

    Article  CAS  PubMed  Google Scholar 

  14. Demple, B. & Halbrook, J. Inducible repair of oxidative DNA damage in Escherichia coli. Nature 304, 466–468 (1983).

    Article  CAS  PubMed  Google Scholar 

  15. Christman, M. F., Morgan, R. W., Jacobson, F. S. & Ames, B. N. Positive control of a regulon for defences against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41, 753–762 (1985).

    Article  CAS  PubMed  Google Scholar 

  16. Farr, S. B., Natvig, D. O. & Kogoma, T. Toxicity and mutagenicity of plumbagin and the induction of a possible new DNA repair pathway in Escherichia coli. J. Bacteriol. 164, 1309–1316 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Morgan, R. W., Christman, M. F., Jacobson, F. S., Storz, G. & Ames, B. N. Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc. Natl Acad. Sci. USA 83, 8059–8063 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. VanBogelen, R. A., Kelley, P. M. & Neidhardt, F. C. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J. Bacteriol. 169, 26–32 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Greenberg, J. T. & Demple, B. A global response induced in Escherichia coli by redox-cycling agents overlaps with that induced by peroxide stress. J. Bacteriol. 171, 3933–3939 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Walkup, L. K. B. & Kogoma, T. Escherichia coli proteins inducible by oxidative stress mediated by the superoxide radical. J. Bacteriol. 171, 1476–1484 (1987).

    Article  Google Scholar 

  21. Griffiths, M., Sistrom, W. R., Cohen-Bazire, G. & Stanier, R. Y. Function of carotenoids in photosynthesis. Nature 176, 1211–1214 (1955). This groundbreaking study revealed that carotenoids protect cells from photodynamic destruction.

    Article  CAS  PubMed  Google Scholar 

  22. Cogdell, R. J. & Frank, H. A. How carotenoids function in photosynthetic bacteria. Biochim. Biophys. Acta 895, 63–79 (1987).

    Article  CAS  PubMed  Google Scholar 

  23. Kalai, T., Hideg, E., Vass, I. & Hideg, K. Double (fluorescent and spin) sensors for detection of reactive oxygen species in the thylakoid membrane. Free Radic. Biol. Med. 24, 649–652 (1998).

    Article  CAS  PubMed  Google Scholar 

  24. Glaeser, J. & Klug, G. Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 151, 1927–1938 (2005).

    Article  CAS  PubMed  Google Scholar 

  25. Tandori, J., Hideg, E., Nagy, L., Maroti, P. & Vass, I. Photoinhibition of carotenoidless reaction centers from Rhodobacter sphaeroides by visible light. Effect on protein structure and electron transport. Photosyn. Res. 70, 175–184 (2001).

    Article  CAS  Google Scholar 

  26. Liu, Y. et al. Magnetic field effect on singlet oxygen production in a biochemical system. Chem. Commun. (Camb.) 174–176 (2005).

  27. Arellano, J. B. et al. Formation and geminate quenching of singlet oxygen in purple bacterial reaction center. J. Photochem. Photobiol. B 87, 105–112 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Uchoa, A. F., Knox, P. P., Turchielle, R., Seifullina, N. K. & Baptista, M. S. Singlet oxygen generation in the reaction centers of Rhodobacter sphaeroides. Eur. Biophys. J. 37, 843–850 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Glaeser, J. Zobawa, M., Lottspeich, F. & Klug, G. Protein synthesis patterns reveal a complex regulatory response to singlet oxygen in Rhodobacter. J. Proteome Res. 6, 2460–2471 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. Morgan, P. E., Dean, R. T. & Davies, M. J. Protective mechanisms against peptide and protein peroxides generated by singlet oxygen. Free Radic. Biol. Med. 36, 484–496 (2004).

    Article  CAS  PubMed  Google Scholar 

  31. Leisinger, U. et al. The glutathione peroxidase homologous gene from Chlamydomonas reinhartdtii is transcriptionally up-regulated by singlet oxygen. Plant Mol. Biol. 46, 395–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Anthony, J. R., Warczak, K. L. & Donohue, T. J. A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis. Proc. Natl Acad. Sci. USA 102, 6502–6507 (2005). Identified a transcriptional response to 1O 2 in R. sphaeroides, in which σE is a key regulator.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Burchard, R. P. & Dworkin, M. Light-induced lysis and carotenogenesis in Myxococcus xanthus. J. Bacteriol. 91, 535–545 (1966).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Gorham, H. C., McGowan, S. J., Robson, P. R. H. & Hodgson, D. A. Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol. Microbiol. 19, 171–186 (1996).

    Article  CAS  PubMed  Google Scholar 

  35. Browning, D. F., Whitworth, D. E. & Hodgson, D. A. Light-induced carotenogenesis in Myxococcus xanthus: functional characterization of the ECF sigma factors CarQ and antisigma factor CarR. Mol. Microbiol. 48, 237–251 (2003).

    Article  CAS  PubMed  Google Scholar 

  36. Schroeder, W. A. & Johnson, E. A. Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J. Biol. Chem. 270, 18374–18379 (1995).

    Article  CAS  PubMed  Google Scholar 

  37. Agnez-Lima, L. F., Di Mascio, P., Demple, B. & Menck, C. F. M. Singlet molecular oxygen triggers the soxRS regulon of Escherichia coli. Biol. Chem. 382, 1071–1075 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Kim, S. Y., Kim, E. J. & Park, J.-W. Control of singlet oxygen-induced oxidative damage in Escherichia coli. J. Biochem. Mol. Biol. 35, 353–357 (2002).

    CAS  PubMed  Google Scholar 

  39. Saenkham, P., Eiamphungporn, W., Farrand, S. K., Vattanaviboon, P. & Mongkolsuk, S. Multiple superoxide dismutases in Agrobacterium tumefaciens: functional analysis, gene regulation, and influence on tumorigenesis. J. Bacteriol. 189, 8807–8817 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Saenkham, P., Utamapongchai, S., Vattanaviboon, P. & Mongkolsuk, S. Agrobacterium tumefaciens iron superoxide dismutases have protective roles against singlet oxygen toxicity generated from illuminated Rose Bengal. FEMS Microbiol. Lett. 289, 97–103 (2008).

    Article  CAS  PubMed  Google Scholar 

  41. Newman, J. D., Falkowski, M. J., Schilke, B. A., Anthony, L. C. & Donohue, T. J. The Rhodobacter sphaeroides ECF sigma factor, σE, and the target promoters cycA P3 and rpoE P1. J. Mol. Biol. 294, 307–320 (1999).

    Article  CAS  PubMed  Google Scholar 

  42. Newman, J. D., Anthony, J R. & Donohue, T. J. The importance of zinc-binding to the function of Rhodobacter sphaeroides ChrR as an anti-sigma factor. J. Mol. Biol. 313, 485–499 (2001).

    Article  CAS  PubMed  Google Scholar 

  43. Anthony, J. R., Newman, J. D. & Donohue, T. J. Interactions between the Rhodobacter sphaeroides ECF sigma factor, σE, and its anti-sigma factor, ChrR. J. Mol. Biol. 341, 345–360 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Campbell, E. A. et al. A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol. Cell 27, 793–805 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Green, H. A. & Donohue, T. J. Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. J. Bacteriol. 188, 5712–5721 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Braatsch, S., Moskvin, O. V., Klug, G. & Gomelsky, M. Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions. J. Bacteriol. 186, 7726–7735 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Dufour, Y. S., Landick, R. & Donohue, T. J. Organization and evolution of the biological response to singlet oxygen stress. J. Mol. Biol. 383, 713–730 (2008). This article described a new level of understanding of the organization and evolution of 1O 2 stress responses in bacteria, provided by high-throughput experimental studies combined with computational tools.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Nuss, A. M., Glaeser, J. & Klug, G. RpoHII activates oxidative-stress defence systems and is controlled by RpoE in the singlet oxygen-dependent response in Rhodobacter sphaeroides. J. Bacteriol. 191, 220–230 (2009).

    Article  CAS  PubMed  Google Scholar 

  49. Karls, R. K., Brooks, J., Rossmeissl, P., Luedke, J. & Donohue, T. J. Metabolic roles of a Rhodobacter sphaeroides member of the σ32 family. J. Bacteriol. 180, 10–19 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Lonetto, M. A., Brown, K. L., Rudd, K. E. & Buttner, M. J. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial σ factors involved in the regulation of extracytoplasmic functions. Proc. Natl Acad. Sci. USA 91, 7573–7577 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Gruber, T. M. & Gross, C. A. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57, 441–466 (2003).

    Article  CAS  PubMed  Google Scholar 

  52. Battistuzzi, F. U., Feijao, A. & Hedges, S. B. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4, 44–57 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Lourenco, R. F. & Gomes, S. L. The transcriptional response to cadmium, organic hydroperoxide, singlet oxygen and UV-A mediated by the σE-ChrR system in Caulobacter crescentus. Mol. Microbiol. 72, 1159–1170 (2009).

    Article  CAS  PubMed  Google Scholar 

  54. Cronan, J. E. Jr. Phospholipid modifications in bacteria. Curr. Opin. Microbiol. 5, 202–205 (2002).

    Article  CAS  PubMed  Google Scholar 

  55. Hendrischk, A.-K., Braatsch, S., Glaeser, J. & Klug, G. The phrA gene of Rhodobacter sphaeroides encodes a photolyase and is regulated by singlet oxygen and peroxide in a σE-dependent manner. Microbiology 153, 1842–1851 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. Ursini, F. et al. Diversity of glutathione peroxidases. Meth. Enzymol. 252, 38–53 (1995).

    Article  CAS  Google Scholar 

  57. Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498 (2004).

    Article  CAS  PubMed  Google Scholar 

  58. Krieger-Liszkay, A. Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337–346 (2004).

    Article  PubMed  Google Scholar 

  59. Fischer, B. B., Krieger-Liszkay, A. & Eggen, R. I. L. Oxidative stress induced by the photosensitizers neutral red (type I) or rose Bengal (type II) in the light causes different molecular responses in Chlamydomonas reinhardtii. Plant Sci. 168, 747–759 (2005).

    Article  CAS  Google Scholar 

  60. Fischer, B. B., Eggen, R. I. L., Trebst, A. & Krieger-Liszkay, A. The glutathione peroxidase homologous gene Gpxh in Chlamydomonas reinhardtii is upregulated by singlet oxygen in photosystem II. Planta 223, 583–590 (2006).

    Article  CAS  PubMed  Google Scholar 

  61. Ledford, H. K., Chin, B. L. & Niyogi, K. K. Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot. Cell 6, 919–930 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Fischer, B. B. et al. Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett. 581, 5555–5560 (2007).

    Article  CAS  PubMed  Google Scholar 

  63. Zeilstra-Ryalls, J. H. & Kaplan, S. Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm. Cell Mol. Life Sci. 61, 417–436 (2004).

    Article  CAS  PubMed  Google Scholar 

  64. Kaplan, S., Eraso, J. & Roh, J. H. Interacting regulatory networks in the facultative photosynthetic bacterium, Rhodobacter sphaeroides 2.4.1. Biochem. Soc. Trans. 33, 51–55 (2005).

    Article  CAS  PubMed  Google Scholar 

  65. Burgess, R. R., Travers, A. A., Dunn, J. J. & Bautz, E. K. F. Factor stimulating transcription by RNA polymerase. Nature 221 43–46 (1969).

    Article  CAS  PubMed  Google Scholar 

  66. Lonetto, M., Gribskov, M. & Gross, C. A. The σ70 family: sequence conservation and evolutionary relationships. J. Bacteriol. 174, 3843–3849 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Work on the singlet oxygen stress response has been supported by the Department of Energy (DE-FG02-05ER15653) and, more recently, by the National Institutes of General Medical Sciences (GM075273). The authors thank Y.S. Dufour and H.A. Green for allowing us to discuss their unpublished results. We also thank Y. Dufour for advice on the production of Figure 4. Furthermore, we recognize past and current members of the Donohue laboratory for their contribution to the observations summarized in this work.

Author information

Authors and Affiliations

  1. Department of Bacteriology, University of Wisconsin–Madison, 1550 Linden Drive, Madison, 53706, Wisconsin, USA

    Eva C. Ziegelhoffer & Timothy J. Donohue

Authors
  1. Eva C. Ziegelhoffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy J. Donohue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy J. Donohue.

Related links

Related links

DATABASES

Entrez Genome Project

Agrobacterium tumefaciens

Caulobacter crescentus

Chlamydomonas reinhardtii

Escherichia coli

Myxococcus xanthus

Rhodobacter sphaeroides

Salmonella enterica subsp. enterica serovar Typhimurium

FURTHER INFORMATION

Timothy J. Donohue's homepage

Glossary

Diradical

A molecular species with two electrons occupying two degenerate molecular orbitals, typified by high reactivity and a short lifespan.

Fenton reaction

The reaction in which free ferrous iron (Fe2+) transfers an electron to hydrogen peroxide (H2O2) to produce a hydroxyl radical (OH·): H2O2 + Fe2+ → OH− + FeO2+ + H+ → Fe3+ + OH− + OH·

Triplet excited state

The higher energy state of a molecule that is characterized by an electron paramagnetic resonance spectrum with three peaks.

Photosensitizer

A chemical compound that readily undergoes photo-excitation and then transfers its energy to other molecules, resulting in a reaction mixture that is sensitive to light.

Respiratory burst

The rapid release of reactive oxygen species from neutrophils and macrophages of the immune system.

Paraquat

A redox cycling agent that can be oxidized by dioxygen, resulting in the production of superoxide; also called methyl viologen.

Isozymes

Any of the electrophoretically distinct forms of an enzyme, which represent different polymeric states but have the same function.

Carotenoids

A class of pigments that are widely distributed in nature; pigments can be yellow, orange, red or purple.

Photosynthetic reaction centre

A site where molecular excitations originating from light are transformed into a series of electron transfer reactions. It is composed of a multiprotein complex containing pigmented cofactors (such as chlorophyll).

Phototroph

An organism that uses light as a source of metabolic energy.

Dane-Py

(3-(N-diethylaminoethyl)-N-dansyl-aminomethyl-2,5-dihydro-2,2,5,5-tetramethyl-1-H-pyrrole.) A fluorescent molecular trap that is specific for singlet oxygen; excitation occurs at 337 nm, with emission at 545 nm.

Electron paramagnetic resonance spin trapping

Experiments in which a particular electron spin state of a molecule is isolated to measure its spectrum.

σ-factor

A specificity subunit of prokaryotic RNA polymerase that directs the RNA polymerase holoenzyme to the promoter DNA of specific genes. The primary σ-factor in cells is responsible for the recognition of so-called housekeeping genes, and alternative σ-factors are devoted to specialized functions.

Methylene blue

A photosensitizer that is used to generate singlet oxygen when it is exposed to both oxygen and light.

Rose bengal

A widely used stain that also functions as a photosensitizer, specifically to generate singlet oxygen from ground state triplet oxygen.

Position-specific weighted matrix

A statistical representation of patterns in biological sequences, composed of a matrix of score values that gives a weighted match to any given substring of fixed length.

Photolyase

An enzyme that repairs DNA that has been damaged by ultraviolet light exposure by breaking pyrimidine dimers.

Thylakoid

An internal membrane system occupying the main body of a plastid; particularly well-developed in chloroplasts.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ziegelhoffer, E., Donohue, T. Bacterial responses to photo-oxidative stress. Nat Rev Microbiol 7, 856–863 (2009). https://doi.org/10.1038/nrmicro2237

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2237

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing