Skip to main content
Log in

Mechanisms of oxygen regulation in microorganisms

  • Review
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

The review considers the main mechanisms of metabolism regulation that operate in pro- and eukaryotic microorganisms upon changes in the partial pressure of oxygen in the medium, i.e., upon transition from normoxia via hypoxia to anoxia or upon the reverse transition. The involvement in these processes of hemes, the Hap transcription factors, the Rox1 repressor protein, sterols, and other regulatory factors is discussed.

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

References

  1. Waterland, R.A., Basu, A., Chance, B., and Poyton, R.O., The Isoforms of Yeast Cytochrome c Oxidase Subunit V Alter the In Vivo Kinetic Properties of the Holoenzyme, J. Biol. Chem., 1991, vol. 266, pp. 4180–4186.

    PubMed  CAS  Google Scholar 

  2. Burke, P.V., Raitt, D.C., Allen, L.A., Kellogg, E.A., and Poyton, R.O., Effects of Oxygen Concentration on the Expression of Cytochrome c and Cytochrome c Oxidase Genes in Yeast, J. Biol. Chem., 1997, vol. 272, pp. 14705–14712.

    Article  PubMed  CAS  Google Scholar 

  3. Kwast, K.E., Burke, P.V., and Poyton, R.O., Oxygen Sensing and the Transcriptional Regulation of Oxygen Responsive Genes in Yeast, J. Exp. Biol., 1998, vol. 201, pp. 1177–1195.

    PubMed  CAS  Google Scholar 

  4. Davies, B.S.J. and Rine, J., A Role for Sterol Levels in Oxygen Sensing in Saccharomyces cerevisiae, Genetics, 2006, vol. 174, no. 1, pp. 191–201.

    Article  PubMed  CAS  Google Scholar 

  5. Hughes, A.L., Todd, B.L., and Espenshade, P.J., SREBP Pathway Responds to Sterols and Functions as an Oxygen Sensor in Fission Yeast, Cell, 2005, vol. 120, pp. 831–842.

    Article  PubMed  CAS  Google Scholar 

  6. Todd, B.L., Stewart, E.V., Burg, J.S., Hughes, A.L., and Espenshade, P.J., Sterol Regulatory Element Binding Protein Is a Principal Regulator of Anaerobic Gene Expression in Fission Yeast, Mol. Cell. Biol., 2006, vol. 26, no. 7, pp. 2817–2831.

    Article  PubMed  CAS  Google Scholar 

  7. Znaidi, S., Weber, S., Al-Abdin, O.Z., Bomme, P., Saidane, S., Drouin, S., Lemieux, S., De Deken, X., Robert, F., and Raymond, M., Genomewide Location Analysis of Candida albicans Upc2p, a Regulator of Sterol Metabolism and Azole Drug Resistance, Eukaryot. Cell, 2008, vol. 7, no. 5, pp. 836–847.

    Article  PubMed  CAS  Google Scholar 

  8. Bunn, H.F. and Poyton, R.O., Oxygen Sensing and Molecular Adaptation to Hypoxia, Physiol. Rev., 1996, vol. 76, pp. 839–885.

    PubMed  CAS  Google Scholar 

  9. Kwast, K.E., Lai, L.C., Menda, N., James, D.T., Aref, S., and Burke, P.V., Genomic Analyses of Anaerobically Induced Genes in Saccharomyces cerevisiae: Functional Roles of Rox1 and Other Factors in Mediating the Anoxic Response, J. Bacteriol., 2002, vol. 184, no. 1, pp. 250–265.

    Article  PubMed  CAS  Google Scholar 

  10. Lai, L.C., Kosorukoff, A.L., Burke, P.V., and Kwast, K.E., Metabolic-State-Dependent Remodeling of the Transcriptome in Response to Anoxia and Subsequent Reoxygenation in Saccharomyces cerevisiae, Eukaryot. Cell, 2006, vol. 5, no. 9, pp. 1468–1489.

    Article  PubMed  CAS  Google Scholar 

  11. Zitomer, R.S., Limbach, M.P., Rodriguez-Torres, A.M., Balasubramanian, B., Deckert, J., and Snow, P.M., Approaches to the Study of Rox1 Repression of the Hypoxic Genes in the Yeast Saccharomyces cerevisiae, Methods, 1997, vol. 11, pp. 279–288.

    Article  PubMed  CAS  Google Scholar 

  12. Knijnenburg, T.A., de Winde, J.H., Daran, J.-M., Daran-Lapujade, P., Pronk, J.T., Reinders, M.J.T., and Wessels, L.F.A., Exploiting Combinatorial Cultivation Conditions To Infer Transcriptional Regulation, BMC Genomics, 2007, vol. 8 P, p. 25.

    Article  CAS  Google Scholar 

  13. Laz, T.M., Pietras, D.F., and Sherman, F., Differential Regulation of the Duplicated Iso-Cytochrome c Genes in Yeast, Proc. Natl. Acad. Sci. USA, 1984, vol. 81, pp. 4475–4479.

    Article  PubMed  CAS  Google Scholar 

  14. Hon, T., Lee, H.C., Hach, A., Johnson, J.L., Craig, E.A., Erdjument-Bromage, H., Tempst, P., and Zhang, L., The Hsp70-Ydj1 Molecular Chaperone Represses the Activity of the Heme Activator Protein Hap1 in the Absence of Heme, Mol. Cell. Biol., 2001, vol. 21, pp. 7923–7932.

    Article  PubMed  CAS  Google Scholar 

  15. Lan, C., Lee, H.C., Tang, S., and Zhang, L., A Novel Mode of Chaperone Action: Heme Activation of Hap1 by Enhanced Association of Hsp90 with the Repressed Hsp70-Hap1 Complex, J. Biol. Chem., 2004, vol. 279, pp. 27607–27612.

    Article  PubMed  CAS  Google Scholar 

  16. Lee, H.C., Hon, T., and Zhang, L., The Molecular Chaperone Hsp90 Mediates Heme Activation of the Yeast Transcriptional Activator Hap1, J. Biol. Chem., 2002, vol. 277, pp. 7430–7437.

    Article  PubMed  CAS  Google Scholar 

  17. Hon, T., Dodd, A., Dirmeier, R., Gorman, N., Sinclair, P.R., Zhang, L., and Poyton, R.O., Multiple Oxygen-Responsive Steps in the Heme Biosynthetic Pathway Affect Hap1 Activity, J. Biol. Chem., 2003, vol. 278, no. 50, pp. 50771–50780.

    Article  PubMed  CAS  Google Scholar 

  18. Hickman, M.J. and Winston, F., Heme Levels Switch the Function of Hap1 of Saccharomyces cerevisiae between Transcriptional Activator and Transcriptional Repressor, Mol. Cell. Biol., 2007, vol. 27, no. 21, pp. 7414–7424.

    Article  PubMed  CAS  Google Scholar 

  19. Hon, T., Lee, H.C., Hu, Z., Iyer, V.R., and Zhang, L., The Heme Activator Protein Hap1 Represses Transcription by a Heme-Independent Mechanism in Saccharomyces cerevisiae, Genetics, 2005, vol. 169, pp. 1343–1352.

    Article  PubMed  CAS  Google Scholar 

  20. Keleher, C.A., Redd, M.J., Schultz, J., Carlson, M., and Johnson, A.D., Ssn6-Tup1 Is a General Repressor of Transcription in Yeast, Cell, 1992, vol. 68, pp. 709–719.

    Article  PubMed  CAS  Google Scholar 

  21. Sertil, O., Kapoor, R., Cohen, B.D., Abramova, N., and Lowry, C.V., Synergistic Repression of Anaerobic Genes by Mot3 and Rox1 in Saccharomyces cerevisiae, Nucleic Acids Res., 2003, vol. 31, no. 20, pp. 5831–5837.

    Article  CAS  Google Scholar 

  22. Tzamarias, D. and Struhl, K., Distinct TPR Motifs of Cyc8 Are Involved in Recruiting the Cyc8-Tup1 Corepressor Complex to Differentially Regulated Promoters, Genes Dev., 1995, vol. 9, pp. 821–831.

    Article  PubMed  CAS  Google Scholar 

  23. Varanasi, U.S., Klis, M., Mikesell, P.B., and Trumbly, R.J., The Cyc8(Ssn6)-Tup1 Corepressor Complex Is Composed of One Cyc8 and Four Tup1 Subunits, Mol. Cell. Biol., 1996, vol. 16, pp. 6707–6714.

    PubMed  CAS  Google Scholar 

  24. Lee, T.I., Rinaldi, N.J., Robert, F., Odom, D.T., Bar-Joseph, Z., Gerber, G.K., Hannett, N.M., Harbison, C.T., Thompson, C.M., Simon, I., Zeitlinger, J., Jennings, E.G., Murray, H.L., Gordon, D.B., Ren, B., Wyrick, J.J., Tagne, J.B., Volkert, T.L., Fraenkel, E., Gifford, D.K., and Young, R.A., Transcriptional Regulatory Networks in Saccharomyces cerevisiae, Science, 2002, vol. 298, no. 5594, pp. 799–804.

    Article  PubMed  CAS  Google Scholar 

  25. Kastaniotis, A.J., Mennella, T.A., Konrad, C., Torres, A.M., and Zitomer, R.S., Roles of Transcription Factor Mot3 and Chromatin in Repression of the Hypoxic Gene ANB1 in Yeast, Mol. Cell. Biol., 2000, vol. 20, pp. 7088–7098.

    Article  PubMed  CAS  Google Scholar 

  26. Abramova, N.E., Cohen, B.D., Sertil, O., Kapoor, R., Davies, K.J., and Lowry, C.V., Regulatory Mechanisms Controlling Expression of the dan/tir Mannoprotein Genes during Anaerobic Remodeling of the Cell Wall in Saccharomyces cerevisiae, Genetics, 2001, vol. 157, pp. 1169–1177.

    PubMed  CAS  Google Scholar 

  27. Gustafsson, C.M., Myers, L.C., Li, Y., Redd, M.J., Lui, M., Erdjument-Bromage, H., Tempst, P., and Kornberg, R.D., Identification of Rox3 as a Component of Mediator and RNA Polymerase II Holoenzyme, J. Biol. Chem., 1997, vol. 272, pp. 48–50.

    Article  PubMed  CAS  Google Scholar 

  28. Grishin, A.V., Rothenberg, M., Downs, M.A., and Blumer, K.J., Mot3, a Zn-Finger Transcription Factor That Modulates Gene Expression and Attenuates Mating Pheromone Signaling in Saccharomyces cerevisiae, Genetics, 1998, vol. 149, pp. 879–892.

    PubMed  CAS  Google Scholar 

  29. Abramova, N.E., Sertil, O., Mehta, S., and Lowry, C.V., Reciprocal Regulation of Anaerobic and Aerobic Cell Wall Mannoprotein Gene Expression in Saccharomyces cerevisiae, J. Bacteriol., 2001, vol. 183, pp. 2881–2887.

    Article  PubMed  CAS  Google Scholar 

  30. Sertil, O., Vemula, A., Salmon, S.L., Morse, R.H., and Lowry, C.V., Direct Role for the Rpd3 Complex in Transcriptional Induction of the Anaerobic dan/tir Genes in Yeast, Mol. Cell. Biol., 2007, vol. 27, no. 6, pp. 2037–2047.

    Article  PubMed  CAS  Google Scholar 

  31. Fedoroff, N., Redox Regulatory Mechanisms in Cellular Stress Responses, Ann. Botany, 2006, vol. 98, pp. 289–300.

    Article  CAS  Google Scholar 

  32. Oktyabrsky, O.N. and Smirnova, G.V., Redox Regulation of Cellular Functions, Biokhimiya, 2007, vol. 72, no. 2, pp. 158–174 [Biochemistry (Moscow) (Engl. Transl.), vol. 72, no. 2, pp. 132–145].

    Google Scholar 

  33. Krantz, M., Nordlander, B., Valadi, H., Johansson, M., Gustafsson, L., and Hohmann, S., Anaerobicity Prepares Saccharomyces cerevisiae Cells for Faster Adaptation to Osmotic Shock, Eukaryot. Cell, 2004, vol. 3, no. 6, pp. 1381–1390.

    Article  PubMed  CAS  Google Scholar 

  34. Bourdineaud, J.P., De Sampaio, G., and Lauquin, G.J., A Rox1-Independent Hypoxic Pathway in Yeast. Antagonistic Action of the Repressor Ord1 and Activator Yap1 for Hypoxic Expression of the srp1/tir1 Gene, Mol. Microbiol., 2000, vol. 38, pp. 879–890.

    Article  PubMed  CAS  Google Scholar 

  35. Jiang, Y., Vasconcelles, M.J., Wretzel, S., Light, A., Martin, C.E., and Goldberg, M.A., MGA2 Is Involved in the Low-Oxygen Response Element-Dependent Hypoxic Induction of Genes in Saccharomyces cerevisiae, Mol. Cell. Biol., 2001, vol. 21, no. 18, pp. 6161–6169.

    Article  PubMed  CAS  Google Scholar 

  36. Jiang, Y., Vasconcelles, M.J., Wretzel, S., Light, A., Gilooly, L., McDaid, K., Oh, C.-S., Martin, C.E., and Goldberg, M.A., Mga2p Processing by Hypoxia and Unsaturated Fatty Acids in Saccharomyces cerevisiae: Impact on LORE-Dependent Gene Expression, Eukaryot. Cell, 2002, vol. 1, no. 3, pp. 481–490.

    Article  PubMed  CAS  Google Scholar 

  37. Moskvin, O.V., Kaplan, S., Gilles-Gonzalez, M.A., and Gomelsky, M., Novel Heme-Based Oxygen Sensor with a Revealing Evolutionary History, J. Biol. Chem., 2007, vol. 282, no. 39, pp. 28740–28748.

    Article  PubMed  CAS  Google Scholar 

  38. Gilles-Gonzalez, M.A., Gonzalez, G.., Perutz, M.F., Kiger, L., Marden, M.C., and Poyart, C., Heme-Based Sensors, Exemplified by the Kinase FixL, Are a New Class of Heme Protein with Distinctive Ligand Binding and Autoxidation, Biochemistry, 1994, vol. 33, pp. 8067–8073.

    Article  PubMed  CAS  Google Scholar 

  39. Gilles-Gonzalez, M.A. and Gonzalez, G., Signal Transduction by Heme-Containing PAS-Domain Proteins, J. Appl. Physiol., 2004, vol. 96, pp. 774–783.

    Article  PubMed  CAS  Google Scholar 

  40. Gong, W., Hao, B., Mansy, S.S., Gonzalez, G., Gilles-Gonzalez, M.A., and Chan, M.K., Structure of a Biological Oxygen Sensor: a New Mechanism for Heme-Driven Signal Transduction, Proc. Natl. Acad. USA, 1998, vol. 95, pp. 15177–15182.

    Article  CAS  Google Scholar 

  41. Sousa, E.E.S., Tuckerman, J.R., Gonzalez, G., and Gilles-Gonzalez, M.A., DosT and DevS Are Oxygen-Switched Kinases in Mycobacterium tuberculosis, Protein Sci., 2007, vol. 16, pp. 1708–1719.

    Article  PubMed  CAS  Google Scholar 

  42. Cho, B.K., Knight, E.M., and Palsson, B.O., Transcriptional Regulation of the fad Regulon Genes of Escherichia coli by ArcA, Microbiology (UK), 2006, vol. 152, pp. 2207–2219.

    Article  CAS  Google Scholar 

  43. Partridge, J.D., Sanguinetti, G., Dibden, D.P., Roberts, R.E., Poole, R.K., and Green, J., Transition of Escherichia coli from Aerobic to Micro-Aerobic Conditions Involves Fast and Slow Reacting Regulatory Components, J. Biol. Chem., 2007, vol. 282, no. 15, pp. 11230–11237.

    Article  PubMed  CAS  Google Scholar 

  44. Salmon, K.A., Hung, S.-P., Steffen, N.R., Krupp, R., Baldi, P., Hatfield, G.W., and Gunsalusa, R.P., Global Gene Expression Profiling in Escherichia coli K12. Effects of Oxygen Availability and AcrA, J. Biol. Chem., 2005, vol. 280, no. 15, pp. 15084–15096.

    Article  PubMed  CAS  Google Scholar 

  45. Webster, K.A., Evolution of the Coordinate Regulation of Glycolytic Enzyme Genes by Hypoxia, J. Exp. Biol., 2003, vol. 206, pp. 2911–2922.

    Article  PubMed  CAS  Google Scholar 

  46. Constantinidou, C., Hobman, J.L., Griffiths, L., Patel, M.D., Penn, C.W., Cole, J.A., and Overton, T.W., A Reassessment of the FNR Regulon and Transcriptomic Analysis of the Effects of Nitrate, Nitrite, NarXL, and NarQP as Escherichia coli K12 Adapts from Aerobic to Anaerobic Growth, J. Biol. Chem., 2006, vol. 281, no. 8, pp. 4802–4815.

    Article  PubMed  CAS  Google Scholar 

  47. Fink, R.C., Evans, M.R., Porwollik, S., Vazquez-Torres, A., Jones-Carson, J., Troxell, B., Libby, S.J., McClelland, M., and Hassan, H.M., FNR Is a Global Regulator of Virulence and Anaerobic Metabolism in Salmonella enterica Serovar Typhimurium (ATCC 14028s), J. Bacteriol., 2007, vol. 189, no. 6, pp. 2262–2273.

    Article  PubMed  CAS  Google Scholar 

  48. Whitehead, R.N., Overton, T.W., Snyder, L.A., McGowan, S.J., Smith, H., Cole, J.A., and Saunders, N.J., The Small FNR Regulon of Neisseria gonorrhoeae: Comparison with the Larger Escherichia coli FNR Regulon and Interaction with the NarQ-NarP Regulon, BMC Genomics, 2007, vol. 29, pp. 8–35.

    Google Scholar 

  49. Arzumanyan, V.G., Voronina, N.A., Geidebrekht, O.V., Shelemekh, O.V., Plakunov, V.K., and Belyaev, S.S., Antagonistic Interactions between Stress Factors during the Growth of Microorganisms under Conditions Simulating the Parameters of Their Natural Ecotopes, Mikrobiologiya, 2002, vol. 71, no. 2, pp. 160–165 [Microbiology (Engl. Transl.), vol. 71, no. 2, pp. 133–138].

    Google Scholar 

  50. Heidebrecht, O.V., Arzumanyan, V.G., Plakunov, V.K., and Belyaev S.S., Influence of the Degree of Aeration on Halotolerance of Yeasts of the Genera Candida, Rhodotorula, and Malassezia, Mikrobiologiya, 2003, vol. 72, no. 3, pp. 312–319 [Microbiology (Engl. Transl.), vol. 72, no. 3, pp. 270–276].

    Google Scholar 

  51. Arzumanyan, V.G., Voronina, N.A., Plakunov, V.K., and Belyaev, S.S., The Degree of Halophily in Rhodococcus erythropolis and Halobacterium salinarum Depends on the Partial Pressure of Oxygen, Mikrobiologiya, 2000, vol. 69, no. 2, pp. 290–292 [Microbiology (Engl. Transl.), vol. 69, no. 2, p. 238–240].

    Google Scholar 

  52. Shelemekh O.V., Heidebrecht O.V., Plakunov V.K., Belyaev S.S. “Oxygen Regulation” of the Respiratory Chain Composition in the Yeast Debaryomyces hansenii under Multiple Stress, Mikrobiologiya, 2006, vol. 75, no. 4. [Microbiology (Engl. Transl.), vol. 75, no. 4, pp. 486–493].

  53. Shelemekh, O.V., Reactions of Microorganisms to Simultaneous Impacts of Several Stress Factors: Hypoand Hyperosmotic Conditions, Hypoxia, and Unfavorable Values of pH, Cand. Sci. (Biol.) Dissertation, Moscow: Inst. Microbiol., Russ. Acad. Sci., 2008.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. K. Plakunov.

Additional information

Original Russian Text © V.K. Plakunov, O.V. Shelemekh, 2009, published in Mikrobiologiya, 2009, Vol. 78, No. 5, pp. 592–604.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Plakunov, V.K., Shelemekh, O.V. Mechanisms of oxygen regulation in microorganisms. Microbiology 78, 535–546 (2009). https://doi.org/10.1134/S0026261709050026

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261709050026

Key words

Navigation