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Volume 157, Issue 9

Oxygen reduction in the strict anaerobe Hildenborough: characterization of two membrane-bound oxygen reductases Free

Abstract

Although Hildenborough (DvH) is a strictly anaerobic bacterium, it is able to consume oxygen in different cellular compartments, including extensive periplasmic O reduction with hydrogen as electron donor. The genome of DvH revealed the presence of and genes, encoding a quinol oxidase and a cytochrome oxidase, respectively. In the membranes of DvH, we detected both quinol oxygen reductase [inhibited by heptyl-hydroxyquinoline--oxide (HQNO)] and cytochrome oxidase activities. Spectral and HPLC data for the membrane fraction revealed the presence of -, - and type haems, in addition to a majority of -type haems, but no -type haem, in agreement with carbon monoxide-binding analysis. The cytochrome oxidase is thus of the (/) type, a type not previously described. The monohaem cytochrome is an electron donor to the cytochrome oxidase; its encoding gene is located upstream of the operon and is 50-fold more transcribed than encoding the cytochrome oxidase subunit I. Even when DvH is grown under anaerobic conditions in lactate/sulfate medium, the two terminal oxidase-encoding genes are expressed. Furthermore, the quinol oxidase -encoding genes are more highly expressed than the genes. The operon exhibits an atypical genomic organization, with the gene located downstream of . The occurrence of these membrane-bound oxygen reductases in other strictly anaerobic Deltaproteobacteria is discussed.

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  • Accepted:
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© 2011 SGM
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2011-09-01
2024-04-26
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References

  1. Abdollahi H., Wimpenny J. ( 1990). Effects of oxygen on the growth of Desulfovibrio desulfuricans . J Gen Microbiol 136:1025–1030 [CrossRef]
     [Google Scholar]
  2. Baumgarten A., Redenius I., Kranczoch J., Cypionka H. ( 2001). Periplasmic oxygen reduction by Desulfovibrio species. Arch Microbiol 176:306–309 [View Article][PubMed]
     [Google Scholar]
  3. Bickar D., Bonaventura C., Bonaventura J. ( 1984). Carbon monoxide-driven reduction of ferric heme and heme proteins. J Biol Chem 259:10777–10783[PubMed]
     [Google Scholar]
  4. Bradford M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [View Article][PubMed]
     [Google Scholar]
  5. Brioukhanov A. L., Durand M. C., Dolla A., Aubert C. ( 2010). Response of Desulfovibrio vulgaris Hildenborough to hydrogen peroxide: enzymatic and transcriptional analyses. FEMS Microbiol Lett 310:175–181 [View Article][PubMed]
     [Google Scholar]
  6. Cobine P. A., Pierrel F., Winge D. R. ( 2006). Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta 1763:759–772 [View Article][PubMed]
     [Google Scholar]
  7. Cypionka H. ( 2000). Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54:827–848 [View Article][PubMed]
     [Google Scholar]
  8. Cypionka H., Widdel F., Pfennig N. ( 1985). Survival of sulfate-reducing bacteria after oxygen stress, and growth in sulfate-free oxygen sulfide gradients. FEMS Microbiol Ecol 31:39–45 [View Article]
     [Google Scholar]
  9. Dannenberg S., Kroder M., Dilling W., Cypionka H. ( 1992). Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to reduction of O2 or nitrate by sulfate-reducing bacteria. Arch Microbiol 158:93–99 [View Article]
     [Google Scholar]
  10. Dolla A., Fournier M., Dermoun Z. ( 2006). Oxygen defense in sulfate-reducing bacteria. J Biotechnol 126:87–100 [View Article][PubMed]
     [Google Scholar]
  11. Dolla A., Kurtz D. M., Teixeira M., Voordouw G. ( 2007). Biochemical, proteomic and genetic characterization of oxygen survival mechanisms in sulphate-reducing bacteria of the genus Desulfovibrio . Sulphate-Reducing Bacteria, Environmental and Engineered Systems185–214 Barton L. L., Hamilton W. A. Cambridge, UK: Cambridge University Press; [View Article]
     [Google Scholar]
  12. Fareleira P., Santos B. S., António C., Moradas-Ferreira P., LeGall J., Xavier A. V., Santos H. ( 2003). Response of a strict anaerobe to oxygen: survival strategies in Desulfovibrio gigas . Microbiology 149:1513–1522 [View Article][PubMed]
     [Google Scholar]
  13. Fournier M., Dermoun Z., Durand M. C., Dolla A. ( 2004). A new function of the Desulfovibrio vulgaris Hildenborough [Fe] hydrogenase in the protection against oxidative stress. J Biol Chem 279:1787–1793 [View Article][PubMed]
     [Google Scholar]
  14. Fournier M., Aubert C., Dermoun Z., Durand M. C., Moinier D., Dolla A. ( 2006). Response of the anaerobe Desulfovibrio vulgaris Hildenborough to oxidative conditions: proteome and transcript analysis. Biochimie 88:85–94 [View Article][PubMed]
     [Google Scholar]
  15. Frazão C., Silva G., Gomes C. M., Matias P., Coelho R., Sieker L., Macedo S., Liu M. Y., Oliveira S. et al. ( 2000). Structure of a dioxygen reduction enzyme from Desulfovibrio gigas . Nat Struct Biol 7:1041–1045 [View Article][PubMed]
     [Google Scholar]
  16. Fröhlich J., Sass H., Babenzien H. D., Kuhnigk T., Varma A., Saxena S., Nalepa C., Pfeiffer P., König H. ( 1999). Isolation of Desulfovibrio intestinalis sp. nov. from the hindgut of the lower termite Mastotermes darwiniensis . Can J Microbiol 45:145–152[PubMed] [CrossRef]
     [Google Scholar]
  17. Heidelberg J. F., Seshadri R., Haveman S. A., Hemme C. L., Paulsen I. T., Kolonay J. F., Eisen J. A., Ward N., Methe B. et al. ( 2004). The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22:554–559 [View Article][PubMed]
     [Google Scholar]
  18. Ito T., Okabe S., Satoh H., Watanabe Y. ( 2002). Successional development of sulfate-reducing bacterial populations and their activities in a wastewater biofilm growing under microaerophilic conditions. Appl Environ Microbiol 68:1392–1402 [View Article][PubMed]
     [Google Scholar]
  19. Jensen L. J., Kuhn M., Stark M., Chaffron S., Creevey C., Muller J., Doerks T., Julien P., Roth A. et al. ( 2009). STRING 8–a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37:Database issueD412–D416 [View Article][PubMed]
     [Google Scholar]
  20. Johnson M. S., Zhulin I. B., Gapuzan M. E., Taylor B. L. ( 1997). Oxygen-dependent growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough. J Bacteriol 179:5598–5601[PubMed]
     [Google Scholar]
  21. Jünemann S. ( 1997). Cytochrome bd terminal oxidase. Biochim Biophys Acta 1321:107–127[PubMed] [CrossRef]
     [Google Scholar]
  22. Kawasaki S., Watamura Y., Ono M., Watanabe T., Takeda K., Niimura Y. ( 2005). Adaptive responses to oxygen stress in obligatory anaerobes Clostridium acetobutylicum and Clostridium aminovalericum . Appl Environ Microbiol 71:8442–8450 [View Article][PubMed]
     [Google Scholar]
  23. Kawasaki S., Sakai Y., Takahashi T., Suzuki I., Niimura Y. ( 2009). O2 and reactive oxygen species detoxification complex, composed of O2-responsive NADH : rubredoxin oxidoreductase-flavoprotein A2-desulfoferrodoxin operon enzymes, rubperoxin, and rubredoxin, in Clostridium acetobutylicum . Appl Environ Microbiol 75:1021–1029 [View Article][PubMed]
     [Google Scholar]
  24. Kitamura M., Mizugai K., Taniguchi M., Akutsu H., Kumagai I., Nakaya T. ( 1995). A gene encoding a cytochrome c oxidase-like protein is located closely to the cytochrome c-553 gene in the anaerobic bacterium, Desulfovibrio vulgaris (Miyazaki F). Microbiol Immunol 39:75–80[PubMed] [CrossRef]
     [Google Scholar]
  25. Kjeldsen K. U., Joulian C., Ingvorsen K. ( 2004). Oxygen tolerance of sulfate-reducing bacteria in activated sludge. Environ Sci Technol 38:2038–2043 [View Article][PubMed]
     [Google Scholar]
  26. Kjeldsen K. U., Joulian C., Ingvorsen K. ( 2005). Effects of oxygen exposure on respiratory activities of Desulfovibrio desulfuricans strain DvO1 isolated from activated sludge. FEMS Microbiol Ecol 53:275–284 [View Article][PubMed]
     [Google Scholar]
  27. Krekeler D., Sigalevich P., Teske A., Cypionka H., Cohen Y. ( 1997). A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov. Arch Microbiol 167:369–375 [View Article]
     [Google Scholar]
  28. Kuhnigk T., Branke J., Krekeler D., Cypionka H., Koenig H. ( 1996). A feasible role of sulfate-reducing bacteria in the termite gut. Syst Appl Microbiol 19:139–149 [CrossRef]
     [Google Scholar]
  29. Lauraeus M., Haltia T., Saraste M., Wikström M. ( 1991). Bacillus subtilis expresses two kinds of haem-A-containing terminal oxidases. Eur J Biochem 197:699–705 [View Article][PubMed]
     [Google Scholar]
  30. Le Fourn C., Fardeau M. L., Ollivier B., Lojou E., Dolla A. ( 2008). The hyperthermophilic anaerobe Thermotoga maritima is able to cope with limited amount of oxygen: insights into its defence strategies. Environ Microbiol 10:1877–1887 [View Article][PubMed]
     [Google Scholar]
  31. Lemos R. S., Gomes C. M., Santana M., LeGall J., Xavier A. V., Teixeira M. ( 2001). The ‘strict’ anaerobe Desulfovibrio gigas contains a membrane-bound oxygen-reducing respiratory chain. FEBS Lett 496:40–43 [View Article][PubMed]
     [Google Scholar]
  32. Lobo S. A., Almeida C. C., Carita J. N., Teixeira M., Saraiva L. M. ( 2008). The haem-copper oxygen reductase of Desulfovibrio vulgaris contains a dihaem cytochrome c in subunit II. Biochim Biophys Acta 1777:1528–1534 [View Article][PubMed]
     [Google Scholar]
  33. Lübben M., Morand K. ( 1994). Novel prenylated hemes as cofactors of cytochrome oxidases. Archaea have modified hemes A and O. J Biol Chem 269:21473–21479[PubMed]
     [Google Scholar]
  34. Marschall C., Frenzel C., Cypionka H. ( 1993). Influence of oxygen on sulphate reduction and growth on sulfate-reducing bacteria. Arch Microbiol 159:168–173 [View Article]
     [Google Scholar]
  35. Methé B. A., Nelson K. E., Eisen J. A., Paulsen I. T., Nelson W., Heidelberg J. F., Wu D., Wu M., Ward N. et al. ( 2003). Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302:1967–1969 [View Article][PubMed]
     [Google Scholar]
  36. Mukhopadhyay A., Redding A. M., Joachimiak M. P., Arkin A. P., Borglin S. E., Dehal P. S., Chakraborty R., Geller J. T., Hazen T. C. et al. ( 2007). Cell-wide responses to low-oxygen exposure in Desulfovibrio vulgaris Hildenborough. J Bacteriol 189:5996–6010 [View Article][PubMed]
     [Google Scholar]
  37. Mussmann M., Ishii K., Rabus R., Amann R. ( 2005). Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ Microbiol 7:405–418 [View Article][PubMed]
     [Google Scholar]
  38. Ozawa K., Mogi T., Suzuki M., Kitamura M., Nakaya T., Anraku Y., Akutsu H. ( 1997). Membrane-bound cytochromes in a sulfate-reducing strict anaerobe Desulfovibrio vulgaris Miyazaki F. Anaerobe 3:339–346 [View Article][PubMed]
     [Google Scholar]
  39. Pereira P. M., Teixeira M., Xavier A. V., Louro R. O., Pereira I. A. ( 2006). The Tmc complex from Desulfovibrio vulgaris Hildenborough is involved in transmembrane electron transfer from periplasmic hydrogen oxidation. Biochemistry 45:10359–10367 [View Article][PubMed]
     [Google Scholar]
  40. Pfaffl M. W., Horgan G. W., Dempfle L. ( 2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36
     [Google Scholar]
  41. Pitcher R. S., Brittain T., Watmough N. J. ( 2002). Cytochrome cbb 3 oxidase and bacterial microaerobic metabolism. Biochem Soc Trans 30:653–658 [View Article][PubMed]
     [Google Scholar]
  42. Postgate J. ( 1984). The Sulphate-Reducing Bacteria, 2nd edn. Cambridge, UK: Cambridge University Press;
     [Google Scholar]
  43. Ravenschlag K., Sahm K., Knoblauch C., Jørgensen B. B., Amann R. ( 2000). Community structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine arctic sediments. Appl Environ Microbiol 66:3592–3602 [View Article][PubMed]
     [Google Scholar]
  44. Santana M. ( 2008). Presence and expression of terminal oxygen reductases in strictly anaerobic sulfate-reducing bacteria isolated from salt-marsh sediments. Anaerobe 14:145–156 [View Article][PubMed]
     [Google Scholar]
  45. Santos H., Fareleira P., Xavier A. V., Chen L., Liu M. Y., LeGall J. ( 1993). Aerobic metabolism of carbon reserves by the “obligate anaerobe” Desulfovibrio gigas . Biochem Biophys Res Commun 195:551–557 [View Article][PubMed]
     [Google Scholar]
  46. Sass H., Berchtold M., Branke J., König H., Cypionka H., Babenzien H. D. ( 1998a). Psychrotolerant sulfate-reducing bacteria from an oxic freshwater sediment, description of Desulfovibrio cuneatus sp. nov. and Desulfovibrio litoralis sp. nov. Syst Appl Microbiol 21:212–219[PubMed] [CrossRef]
     [Google Scholar]
  47. Sass H., Wieringa E., Cypionka H., Babenzien H. D., Overmann J. ( 1998b). High genetic and physiological diversity of sulfate-reducing bacteria isolated from an oligotrophic lake sediment. Arch Microbiol 170:243–251 [View Article][PubMed]
     [Google Scholar]
  48. Sass A. M., Eschemann A., Kühl M., Thar R., Sass H., Cypionka H. ( 2002). Growth and chemosensory behavior of sulfate-reducing bacteria in oxygen-sulfide gradients. FEMS Microbiol Ecol 40:47–54[PubMed]
     [Google Scholar]
  49. Sigalevich P., Cohen Y. ( 2000). Oxygen-dependent growth of the sulfate-reducing bacterium Desulfovibrio oxyclinae in coculture with Marinobacter sp. strain MB in an aerated sulfate-depleted chemostat. Appl Environ Microbiol 66:5019–5023 [View Article][PubMed]
     [Google Scholar]
  50. Teske A., Ramsing N. B., Habicht K., Fukui M., Küver J., Jørgensen B. B., Cohen Y. ( 1998). Sulfate-reducing bacteria and their activities in cyanobacterial mats of Solar Lake (Sinai, Egypt). Appl Environ Microbiol 64:2943–2951[PubMed]
     [Google Scholar]
  51. Thauer R. K., Stackebrandt E., Hamilton W. A. ( 2007). Energy Metabolism and Phylogenetic Diversity of Sulphate-Reducing Bacteria, 1st edn. Cambridge: Cambridge University Press;
     [Google Scholar]
  52. Venceslau S. S., Lino R. R., Pereira I. A. ( 2010). The Qrc membrane complex, related to the alternative complex III, is a menaquinone reductase involved in sulfate respiration. J Biol Chem 285:22774–22783 [View Article][PubMed]
     [Google Scholar]
  53. Vincent K. A., Parkin A., Lenz O., Albracht S. P., Fontecilla-Camps J. C., Cammack R., Friedrich B., Armstrong F. A. ( 2005). Electrochemical definitions of O2 sensitivity and oxidative inactivation in hydrogenases. J Am Chem Soc 127:18179–18189 [View Article][PubMed]
     [Google Scholar]
  54. Voordouw G., Strang J. D., Wilson F. R. ( 1989). Organization of the genes encoding [Fe] hydrogenase in Desulfovibrio vulgaris subsp. oxamicus Monticello. J Bacteriol 171:3881–3889[PubMed]
     [Google Scholar]
  55. Weber M. M., Matschiner J. T., Peck H. D. ( 1970). Menaquinone-6 in the strict anaerobes Desulfovibrio vulgaris and Desulfovibrio gigas . Biochem Biophys Res Commun 38:197–204 [View Article][PubMed]
     [Google Scholar]
  56. Wildschut J. D., Lang R. M., Voordouw J. K., Voordouw G. ( 2006). Rubredoxin : oxygen oxidoreductase enhances survival of Desulfovibrio vulgaris Hildenborough under microaerophilic conditions. J Bacteriol 188:6253–6260 [View Article][PubMed]
     [Google Scholar]
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Oxygen reduction in the strict anaerobe Desulfovibrio vulgaris Hildenborough: characterization of two membrane-bound oxygen reductases
Microbiology 157, 2720 (2011); https://doi.org/10.1099/mic.0.049171-0
/content/journal/micro/10.1099/mic.0.049171-0
/content/journal/micro/10.1099/mic.0.049171-0
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