1887

Microbiology Society logo

Volume 160, Issue 9

Structure of the respiratory chain: oxygen affinity of electron transport and the role of cytochrome peroxidase Free

Abstract

The genome of the ethanol-producing bacterium encodes a -type terminal oxidase, cytochrome complex and several -type cytochromes, yet lacks sequences homologous to any of the known bacterial cytochrome oxidase genes. Recently, it was suggested that a putative respiratory cytochrome peroxidase, receiving electrons from the cytochrome complex via cytochrome , might function as a peroxidase and/or an alternative oxidase. The present study was designed to test this hypothesis, by construction of a cytochrome peroxidase mutant (Zm6-), and comparison of its properties with those of a mutant defective in the cytochrome subunit of the complex (Zm6-). Disruption of the cytochrome peroxidase gene (ZZ60192) caused a decrease of the membrane NADH peroxidase activity, impaired the resistance of growing culture to exogenous hydrogen peroxide and hampered aerobic growth. However, this mutation did not affect the activity or oxygen affinity of the respiratory chain, or the kinetics of cytochrome reduction. Furthermore, the peroxide resistance and membrane NADH peroxidase activity of strain Zm6- had not decreased, but both the oxygen affinity of electron transport and the kinetics of cytochrome reduction were affected. It is therefore concluded that the cytochrome peroxidase does not terminate the cytochrome branch of , and that it is functioning as a quinol peroxidase.

  • Received:
  • Accepted:
  • Published Online:
Funding
This study was supported by the:
  • Latvian Council of Science (Award 536/2012 and 09.1306 )
  • Royal Society (Award TG102318)
  • Biotechnology and Biological Sciences Research Council
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.081612-0
2014-09-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/9/2045.html?itemId=/content/journal/micro/10.1099/mic.0.081612-0&mimeType=html&fmt=ahah

References

  1. Atack J. M., Kelly D. J. ( 2006). Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv Microb Physiol 52:73–106 [View Article][PubMed]
     [Google Scholar]
  2. Bergersen F. J., Turner G. L. ( 1979). Systems utilizing oxygenated leghemoglobin and myoglobin as sources of free dissolved O2 at low concentrations for experiments with bacteria. Anal Biochem 96:165–174 [View Article][PubMed]
     [Google Scholar]
  3. Bringer S., Finn R. K., Sahm H. ( 1984). Effect of oxygen on the metabolism of Zymomonas mobilis . Arch Microbiol 139:376–381 [View Article]
     [Google Scholar]
  4. Charoensuk K., Irie A., Lertwattanasakul N., Sootsuwan K., Thanonkeo P., Yamada M. ( 2011). Physiological importance of cytochrome c peroxidase in ethanologenic thermotolerant Zymomonas mobilis . J Mol Microbiol Biotechnol 20:70–82 [View Article][PubMed]
     [Google Scholar]
  5. D’Mello R., Hill S., Poole R. K. ( 1994). Determination of the oxygen affinities of terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: cytochrome bd is a low-affinity oxidase. Microbiology 140:1395–1402 [View Article]
     [Google Scholar]
  6. Desiniotis A., Kouvelis V. N., Davenport K., Bruce D., Detter C., Tapia R., Han C., Goodwin L. A., Woyke T. & other authors ( 2012). Complete genome sequence of the ethanol-producing Zymomonas mobilis subsp. mobilis centrotype ATCC 29191. J Bacteriol 194:5966–5967 [View Article][PubMed]
     [Google Scholar]
  7. Dien B. S., Cotta M. A., Jeffries T. W. ( 2003). Bacteria engineered for fuel ethanol production: current status. Appl Microbiol Biotechnol 63:258–266 [View Article][PubMed]
     [Google Scholar]
  8. Kalnenieks U. ( 2006). Physiology of Zymomonas mobilis: some unanswered questions. Adv Microb Physiol 51:73–117 [View Article][PubMed]
     [Google Scholar]
  9. Kalnenieks U., De Graaf A. A., Bringer-Meyer S., Sahm H. ( 1993). Oxidative phosphorylation in Zymomonas mobilis . Arch Microbiol 160:74–79 [CrossRef]
     [Google Scholar]
  10. Kalnenieks U., Galinina N., Bringer-Meyer S., Poole R. K. ( 1998). Membrane d-lactate oxidase in Zymomonas mobilis: evidence for a branched respiratory chain. FEMS Microbiol Lett 168:91–97[PubMed]
     [Google Scholar]
  11. Kalnenieks U., Galinina N., Strazdina I., Kravale Z., Pickford J. L., Rutkis R., Poole R. K. ( 2008). NADH dehydrogenase deficiency results in low respiration rate and improved aerobic growth of Zymomonas mobilis . Microbiology 154:989–994 [View Article][PubMed]
     [Google Scholar]
  12. Korshunov S., Imlay J. A. ( 2010). Two sources of endogenous hydrogen peroxide in Escherichia coli . Mol Microbiol 75:1389–1401 [View Article][PubMed]
     [Google Scholar]
  13. Kouvelis V. N., Saunders E., Brettin T. S., Bruce D., Detter C., Han C., Typas M. A., Pappas K. M. ( 2009). Complete genome sequence of the ethanol producer Zymomonas mobilis NCIMB 11163. J Bacteriol 191:7140–7141 [View Article][PubMed]
     [Google Scholar]
  14. Lau M. W., Gunawan C., Balan V., Dale B. E. ( 2010). Comparing the fermentation performance of Escherichia coli KO11, Saccharomyces cerevisiae 424A(LNH-ST) and Zymomonas mobilis AX101 for cellulosic ethanol production. Biotechnol Biofuels 3:11 [View Article][PubMed]
     [Google Scholar]
  15. Liang C. C., Lee W. C. ( 1998). Characteristics and transformation of Zymomonas mobilis with plasmid pKT230 by electroporation. Bioprocess Eng 19:81–85
     [Google Scholar]
  16. Markwell M. A. K., Haas S. M., Bieber L. L., Tolbert N. E. ( 1978). A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206–210 [View Article][PubMed]
     [Google Scholar]
  17. Meunier B., Madgwick S. A., Reil E., Oettmeier W., Rich P. R. ( 1995). New inhibitors of the quinol oxidation sites of bacterial cytochromes bo and bd . Biochemistry 34:1076–1083 [View Article][PubMed]
     [Google Scholar]
  18. Nakamura S., Hayashi S., Koga K. ( 1976). Effect of periodate oxidation on the structure and properties of glucose oxidase. Biochim Biophys Acta 445:294–308 [View Article][PubMed]
     [Google Scholar]
  19. Pappas K. M., Kouvelis V. N., Saunders E., Brettin T. S., Bruce D., Detter C., Balakireva M., Han C. S., Savvakis G. & other authors ( 2011). Genome sequence of the ethanol-producing Zymomonas mobilis subsp. mobilis lectotype strain ATCC 10988. J Bacteriol 193:5051–5052 [View Article][PubMed]
     [Google Scholar]
  20. Rogers P. L., Lee K. J., Skotnicki M. L., Tribe D. E. ( 1982). Ethanol production by Zymomonas mobilis . Adv Biochem Eng 23:37–84
     [Google Scholar]
  21. Rogers P. L., Jeon Y. J., Lee K. J., Lawford H. G. ( 2007). Zymomonas mobilis for fuel ethanol and higher value products. Adv Biochem Eng Biotechnol 108:263–288[PubMed]
     [Google Scholar]
  22. Sambrook J., Fritsch E. F., Maniatis T. ( 1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory;
     [Google Scholar]
  23. Seo J.-S., Chong H., Park H. S., Yoon K.-O., Jung C., Kim J. J., Hong J. H., Kim H., Kim J.-H. & other authors ( 2005). The genome sequence of the ethanologenic bacterium Zymomonas mobilis ZM4. Nat Biotechnol 23:63–68 [View Article][PubMed]
     [Google Scholar]
  24. Sootsuwan K., Lertwattanasakul N., Thanonkeo P., Matsushita K., Yamada M. ( 2008). Analysis of the respiratory chain in ethanologenic Zymomonas mobilis with a cyanide-resistant bd-type ubiquinol oxidase as the only terminal oxidase and its possible physiological roles. J Mol Microbiol Biotechnol 14:163–175 [View Article][PubMed]
     [Google Scholar]
  25. Strazdina I., Kravale Z., Galinina N., Rutkis R., Poole R. K., Kalnenieks U. ( 2012). Electron transport and oxidative stress in Zymomonas mobilis respiratory mutants. Arch Microbiol 194:461–471 [View Article][PubMed]
     [Google Scholar]
  26. Swings J., De Ley J. ( 1977). The biology of Zymomonas . Bacteriol Rev 41:1–46[PubMed]
     [Google Scholar]
  27. Takashima E., Konishi K. ( 2008). Characterization of a quinol peroxidase mutant in Aggregatibacter actinomycetemcomitans . FEMS Microbiol Lett 286:66–70 [View Article][PubMed]
     [Google Scholar]
  28. Wood P. M. ( 1984). Bacterial proteins with CO-binding b- or c-type haem. Functions and absorption spectroscopy. Biochim Biophys Acta 768:293–317 [View Article][PubMed]
     [Google Scholar]
  29. Yamada H., Takashima E., Konishi K. ( 2007). Molecular characterization of the membrane-bound quinol peroxidase functionally connected to the respiratory chain. FEBS J 274:853–866 [View Article][PubMed]
     [Google Scholar]
  30. Yang S., Tschaplinski T. J., Engle N. L., Carroll S. L., Martin S. L., Davison B. H., Palumbo A. V., Rodriguez M. Jr, Brown S. D. ( 2009). Transcriptomic and metabolomic profiling of Zymomonas mobilis during aerobic and anaerobic fermentations. BMC Genomics 10:34 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.081612-0
Loading
Structure of the Zymomonas mobilis respiratory chain: oxygen affinity of electron transport and the role of cytochrome c peroxidase
Microbiology 160, 2045 (2014); https://doi.org/10.1099/mic.0.081612-0
/content/journal/micro/10.1099/mic.0.081612-0
/content/journal/micro/10.1099/mic.0.081612-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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