CoChat
Sign Up
Cited by 115Metalloenzymes and iron-sulfur proteinsEnzyme Structure and FunctionMicrobial Fuel Cells and Bioremediation

The DOI matches its Crossref record.

A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774

Open access
Pires, Ricardo H, Lourenço, Alexandra I, Morais, Francisco, Teixeira, Miguel, Xavier, António V, Saraiva, Lı́gia M, Pereira, Inês A.C·2003·Biochimica et Biophysica Acta (BBA) - Bioenergetics
DOI 10.1016/s0005-2728(03)00065-3
Open this paper in CoChat — free accountOpen PDF

Abstract

In the anaerobic respiration of sulfate, performed by sulfate-reducing prokaryotes, reduction of the terminal electron acceptor takes place in the cytoplasm. The membrane-associated electron transport chain that feeds electrons to the cytoplasmic reductases is still very poorly characterized. In this study we report the isolation and characterization of a novel membrane-bound redox complex from Desulfovibrio desulfuricans ATCC 27774. This complex is formed by three subunits, and contains two hemes b, two FAD groups and several iron-sulfur centers. The two hemes b are low-spin, with macroscopic redox potentials of +75 and -20 mV at pH 7.6. Both hemes are reduced by menadiol, a menaquinone analogue, indicating a function for this complex in the respiratory electron-transport chain. EPR studies of the as-isolated and dithionite-reduced complex support the presence of a [3Fe-4S](1+/0) center and at least four [4Fe-4S](2+/1+) centers. Cloning of the genes coding for the complex subunits revealed that they form a putative transcription unit and have homology to subunits of heterodisulfide reductases (Hdr). The first and second genes code for soluble proteins that have homology to HdrA, whereas the third gene codes for a novel type of membrane-associated protein that contains both a hydrophobic domain with homology to the heme b protein HdrE and a hydrophilic domain with homology to the iron-sulfur protein HdrC. Homologous operons are found in the genomes of other sulfate-reducing organisms and in the genome of the green-sulfur bacterium Chlorobium tepidum TLS. The isolated complex is the first example of a new family of respiratory complexes present in anaerobic prokaryotes.

Overview

Integrity signals

Registry

Crossref · 10.1016/s0005-2728(03)00065-3

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Two membrane complexes having quinone-interacting subunits, QmoABC and DsrMKJOP, are probable electron donors to AprBA and DsrAB.

    “A link between the two started to emerge with the identification of two membrane complexes having quinone-interacting subunits, QmoABC and DsrMKJOP, as probable electron donors to AprBA and DsrAB [191–193].”

    From Early bioenergetic evolution (2013) · cites this paper as [192]

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 56

  1. Louro, 1998, Functional and mechanistic studies of cytochrome c3 from Desulfovibrio gigas: thermodynamics of a “proton thruster”, Biochemistry, 37, 15808, 10.1021/bi981505t · DOI
  2. Xavier, 2002, A mechano-chemical model for energy transduction in cytochrome c oxidase: the work of a Maxwell's god, FEBS Lett., 532, 261, 10.1016/S0014-5793(02)03692-X · DOI
  3. Odom, 1981, Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp., FEMS Microbiol. Lett., 12, 47, 10.1111/j.1574-6968.1981.tb07609.x · DOI
  4. Maroc, 1970, Menaquinone (MK-6) in the sulfate reducing obligate anaerobe, Desulfovibrio, Biochim. Biophys. Acta, 197, 87, 10.1016/0005-2728(70)90012-5 · DOI
  5. Rossi, 1993, The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex, J. Bacteriol., 175, 4699, 10.1128/jb.175.15.4699-4711.1993 · DOI
  6. Matias, 2002, Sulfate respiration in Desulfovibrio vulgaris Hildenborough: structure of the 16-heme cytochrome c HmcA at 2.5A resolution and a view of its role in transmembrane electron transfer, J. Biol. Chem., 277, 47907, 10.1074/jbc.M207465200 · DOI
  7. Valente, 2001, A membrane-bound cytochrome c3: a type II cytochrome c3 from Desulfovibrio vulgaris Hildenborough, ChemBioChem, 2, 895, 10.1002/1439-7633(20011203)2:12<895::AID-CBIC895>3.0.CO;2-V · DOI
  8. Saraiva, 2001, In the facultative sulphate/nitrate reducer Desulfovibrio desulfuricans ATCC 27774, the nine-haem cytochrome c is part of a membrane-bound redox complex mainly expressed in sulphate-grown cells, Biochim. Biophys. Acta, 1520, 63, 10.1016/S0167-4781(01)00250-0 · DOI
  9. Matias, 1999, The primary and three-dimensional structures of a nine-haem cytochrome c from Desulfovibrio desulfuricans ATCC 27774 reveal a new member of the Hmc family, Structure, 7, 119, 10.1016/S0969-2126(99)80019-7 · DOI
  10. Keon, 1997, Deletion of two downstream genes alters expression of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough, Arch. Microbiol., 167, 376, 10.1007/s002030050458 · DOI
  11. Dolla, 2000, Deletion of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough hampers hydrogen metabolism and low-redox-potential niche establishment, Arch. Microbiol., 174, 143, 10.1007/s002030000183 · DOI
  12. Steger, 2002, Desulfovibrio sp. genes involved in the respiration of sulfate during metabolism of hydrogen and lactate, Appl. Environ. Microbiol., 68, 1932, 10.1128/AEM.68.4.1932-1937.2002 · DOI
  13. Pereira, 1998, Electron transfer between hydrogenases and mono and multiheme cytochromes in Desulfovibrio spp., JBIC, J. Biol. Inorg. Chem., 3, 494, 10.1007/s007750050259 · DOI
  14. Mander, 2002, Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea, Eur. J. Biochem., 269, 1895, 10.1046/j.1432-1033.2002.02839.x · DOI · Paper page
  15. Hedderich, 1999, Anaerobic respiration with elemental sulfur and with disulfides, FEMS Microbiol. Rev., 22, 353, 10.1111/j.1574-6976.1998.tb00376.x · DOI
  16. Hedderich, 1990, Purification and properties of heterodisulfide reductase from Methanobacterium thermoautotrophicum (strain Marburg), Eur. J. Biochem., 193, 255, 10.1111/j.1432-1033.1990.tb19331.x · DOI
  17. Hedderich, 1994, The heterodisulfide reductase from Methanobacterium thermoautotrophicum contains sequence motifs characteristic of pyridine-nucleotide-dependent thioredoxin reductases, Eur. J. Biochem., 225, 253, 10.1111/j.1432-1033.1994.00253.x · DOI
  18. Setzke, 1994, H2: heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum. Composition and properties, Eur. J. Biochem., 220, 139, 10.1111/j.1432-1033.1994.tb18608.x · DOI
  19. Lemos, 2001, Acidianus ambivalens Complex II typifies a novel family of succinate dehydrogenases, Biochem. Biophys. Res. Commun., 281, 141, 10.1006/bbrc.2001.4317 · DOI
  20. Iwasaki, 2002, Novel [2Fe–2S]-type redox center C in SdhC of archaeal respiratory complex II from Sulfolobus tokodaii strain 7, J. Biol. Chem., 277, 39642, 10.1074/jbc.M207312200 · DOI
  21. Kunkel, 1997, Heterodisulfide reductase from methanol-grown cells of Methanosarcina barkeri is not a flavoenzyme, Eur. J. Biochem., 244, 226, 10.1111/j.1432-1033.1997.00226.x · DOI
  22. Simianu, 1998, Purification and properties of the heme- and iron–sulfur-containing heterodisulfide reductase from Methanosarcina thermophila, Biochemistry, 37, 10027, 10.1021/bi9726483 · DOI
  23. Liu, 1981, The isolation of a hexaheme cytochrome from Desulfovibrio desulfuricans and its identification as a new type of nitrite reductase, J. Biol. Chem., 256, 13159, 10.1016/S0021-9258(18)43021-9 · DOI
  24. Fischer, 1964, A simple serum iron method using the new sensitive chromogen trypiridyl-s-triazine, Clin. Chem., 10, 21, 10.1093/clinchem/10.1.21 · DOI
  25. Berry, 1987, Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra, Anal. Biochem., 161, 1, 10.1016/0003-2697(87)90643-9 · DOI
  26. Lubben, 1994, Novel prenylated hemes as cofactors of cytochrome oxidases. Archaea have modified hemes A and O, J. Biol. Chem., 269, 21473, 10.1016/S0021-9258(17)31828-8 · DOI
  27. Aliverti, 1999, vol. 131, 9
  28. Snyder, 1999, Ubiquinone at center N is responsible for triphasic reduction of cytochrome b in the cytochrome bc(1) complex, J. Biol. Chem., 274, 31209, 10.1074/jbc.274.44.31209 · DOI
  29. Gomes, 2001, A new type-II NADH dehydrogenase from the archaeon Acidianus ambivalens: characterization and in vitro reconstitution of the respiratory chain, J. Bioenerg. Biomembranes, 33, 1, 10.1023/A:1005630221892 · DOI
  30. Stams, 1982, Oxygen-labile L(+) lactate dehydrogenase activity in Desulfovibrio desulfuricans, FEMS Microbiol. Lett., 13, 389
  31. Axley, 1991, Catalytic properties of an Escherichia coli formate dehydrogenase mutant in which sulfur replaces selenium, Proc. Natl. Acad. Sci. U. S. A., 88, 8450, 10.1073/pnas.88.19.8450 · DOI
  32. Lester, 1971, Effects of molybdate and selenite on formate and nitrate metabolism in Escherichia coli, J. Bacteriol., 105, 1006, 10.1128/JB.105.3.1006-1014.1971 · DOI
  33. Fritz, 2000, Adenylylsulfate reductases from archaea and bacteria are 1:1 alphabeta-heterodimeric iron–sulfur flavoenzymes—high similarity of molecular properties emphasizes their central role in sulfur metabolism, FEBS Lett., 473, 63, 10.1016/S0014-5793(00)01500-3 · DOI
  34. F.M. Ausubel, R. Brent, R.E. Kingstone, D.D. Moore, J.G. Seidman, J.A. Smith, K. Struhl, Current Protocols in Molecular Biology, Greene Publishing Associates/Wiley Interscience, New York, 1995.
  35. Thompson, 1997, The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res., 25, 4876, 10.1093/nar/25.24.4876 · DOI
  36. Teixeira, 1993, Pitfalls in assigning heme axial coordination by EPR. c-Type cytochromes with atypical Met–His ligation, FEBS Lett., 317, 233, 10.1016/0014-5793(93)81282-5 · DOI
  37. Klenk, 1997, The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus, Nature, 390, 364, 10.1038/37052 · DOI
  38. Eisen, 2002, The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium, Proc. Natl. Acad. Sci. U. S. A., 99, 9509, 10.1073/pnas.132181499 · DOI
  39. Wierenga, 1986, Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint, J. Mol. Biol., 187, 101, 10.1016/0022-2836(86)90409-2 · DOI
  40. Xia, 1997, Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria, Science, 277, 60, 10.1126/science.277.5322.60 · DOI
  41. Lancaster, 1999, Structure of fumarate reductase from Wolinella succinogenes at 2.2A resolution, Nature, 402, 377, 10.1038/46483 · DOI
  42. Jormakka, 2002, Molecular basis of proton motive force generation: structure of formate dehydrogenase-N, Science, 295, 1863, 10.1126/science.1068186 · DOI
  43. Berks, 1995, Sequence analysis of subunits of the membrane-bound nitrate reductase from a denitrifying bacterium: the integral membrane subunit provides a prototype for the dihaem electron-carrying arm of a redox loop, Mol. Microbiol., 15, 319, 10.1111/j.1365-2958.1995.tb02246.x · DOI
  44. Gross, 1998, Identification of histidine residues in Wolinella succinogenes hydrogenase that are essential for menaquinone reduction by H2, Mol. Microbiol., 30, 639, 10.1046/j.1365-2958.1998.01100.x · DOI
  45. Rich, 1999, Generic features of quinone-binding sites, Biochem. Soc. Trans., 27, 561, 10.1042/bst0270561 · DOI
  46. Fisher, 2000, A motif for quinone binding sites in respiratory and photosynthetic systems, J. Mol. Biol., 296, 1153, 10.1006/jmbi.2000.3509 · DOI
  47. Abramson, 2000, The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site, Nat. Struct. Biol., 7, 910, 10.1038/82824 · DOI
  48. Madadi-Kahkesh, 2001, A paramagnetic species with unique EPR characteristics in the active site of heterodisulfide reductase from methanogenic archaea, Eur. J. Biochem., 268, 2566, 10.1046/j.1432-1327.2001.02141.x · DOI
  49. Wood, 1984, Bacterial proteins with CO-binding b- or c-type haem. Functions and absorption spectroscopy, Biochim. Biophys. Acta, 768, 293, 10.1016/0304-4173(84)90020-X · DOI
  50. Jones, 1985, The analysis of cytochromes, Methods Microbiol., 18, 285, 10.1016/S0580-9517(08)70479-3 · DOI
  51. Shelver, 1997, CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein, Proc. Natl. Acad. Sci. U. S. A., 94, 11216, 10.1073/pnas.94.21.11216 · DOI · Paper page
  52. Hagen, 1992, vol. 38, 165
  53. Pereira, 2000, Characterization of a heme c nitrite reductase from a non-ammonifying microorganism, Desulfovibrio vulgaris Hildenborough, Biochim. Biophys. Acta, 1481, 119, 10.1016/S0167-4838(00)00111-4 · DOI
  54. Hendrich, 2001, Correlations of structure and electronic properties from EPR spectroscopy of hydroxylamine oxidoreductase, J. Am. Chem. Soc., 123, 2997, 10.1021/ja002982d · DOI
  55. Richardson, 2000, Bacterial respiration: a flexible process for a changing environment, Microbiology, 146, 551, 10.1099/00221287-146-3-551 · DOI · Paper page
  56. Baumer, 1998, The F420H2:heterodisulfide oxidoreductase system from Methanosarcina species: 2. Hydroxyphenazine mediates electron transfer from F420H2 dehydrogenase to heterodisulfide reductase, FEBS Lett., 428, 295, 10.1016/S0014-5793(98)00555-9 · DOI

Cited by

Sorted by citations

Metadata

Authors
Pires, R. H., Lourenço, A. I., Morais, F., Teixeira, M., Xavier, A. V., Saraiva, L. M., & Pereira, I. A. C.
Affiliations
Universidade Nova de Lisboa (PT)
Corresponding author
Pereira, Inês A.C
ORCID
Venue
Biochimica et Biophysica Acta (BBA) - Bioenergetics
Publisher
Elsevier BV
Published
2003-08
Volume
1605
Issue
1-3
Pages
67-82
ISSN
0005-2728 (ISSN-L)
DOI
10.1016/s0005-2728(03)00065-3
OpenAlex
W2052412394
Cited by
115
References
0
Citations by year
2026: 4 · 2025: 2 · 2024: 5 · 2023: 1 · 2022: 5 · 2021: 4 · 2020: 4 · 2019: 2 · 2018: 7 · 2017: 3 · 2016: 9 · 2015: 4 · 2014: 8 · 2013: 8 · 2012: 10
FWCI
2.28
Type
journal article
Language
en
Open access
Licence
Locations
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics (publishedVersion)
  • PubMed (publishedVersion)
Funders
Fundação para a Ciência e a Tecnologia
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
  • Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
Keywords
Desulfovibrio desulfuricans, sulfate-reducing bacteria, anaerobic respiration, heme b, FAD, iron-sulfur clusters, operon, Chlorobium tepidum, redox potential
MeSH terms
Amino Acid Sequence, Desulfovibrio, Electron Spin Resonance Spectroscopy, Electron Transport, Molecular Sequence Data, Multienzyme Complexes, Oxidoreductases, Spectrophotometry

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review