High-resolution structures of the oxidized and reduced states of cytochrome c554 from Nitrosomonas europaea

Iverson, T.M.; Arciero, David M.; Hooper, Alan B.; Rees, Douglas C.

doi:10.1007/s007750100213

Cited by 50 publications

(51 citation statements)

References 16 publications

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“…Thus, the study of these various proteins yields information on the variety of strategies that Nature can employ to achieve a common function using the same structural arrangement of the redox active sites. This situation is identical to that recently reported for transmembrane cytochrome c ox- idase from Rhodothermus marinus that is capable of pumping protons coupled to the redox cycle, but does not contain "conserved" residues previously considered to be essential for this process (40,41), and to the utilization of similar structural arrangements of heme cofactors in several proteins participating in the ammonia metabolism of Nitrosomonas europaea (42). The integrated analysis of the thermodynamic, structural, and theoretical results reported in this work reveals that the interactions between the centers are organized in a network of cooperativities, which selects particular microscopic states that result in an effective thermodynamic gating for coupling the redox and acid-base cycle.…”

Section: Discussionsupporting

confidence: 84%

Conformational Component in the Coupled Transfer of Multiple Electrons and Protons in a Monomeric Tetraheme Cytochrome

Louro¹,

Bento²,

Matías³

et al. 2001

Journal of Biological Chemistry

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Cell metabolism relies on energy transduction usually performed by complex membrane-spanning proteins that couple different chemical processes, e.g. electron and proton transfer in proton-pumps. There is great interest in determining at the molecular level the structural details that control these energy transduction events, particularly those involving multiple electrons and protons, because tight control is required to avoid the production of dangerous reactive intermediates. Tetraheme cytochrome c 3 is a small soluble and monomeric protein that performs a central step in the bioenergetic metabolism of sulfate reducing bacteria, termed "proton-thrusting," linking the oxidation of molecular hydrogen with the reduction of sulfate. The mechanochemical coupling involved in the transfer of multiple electrons and protons in cytochrome c 3 from Desulfovibrio desulfuricans ATCC 27774 is described using results derived from the microscopic thermodynamic characterization of the redox and acid-base centers involved, crystallographic studies in the oxidized and reduced states of the cytochrome, and theoretical studies of the redox and acid-base transitions. This proton-assisted two-electron step involves very small, localized structural changes that are sufficient to generate the complex network of functional cooperativities leading to energy transduction, while using molecular mechanisms distinct from those established for other Desulfovibrio sp. cytochromes from the same structural family.Recent developments in techniques of structural biology have opened the way for probing the mechanisms used by biological macromolecules involved in energy transduction at the molecular level. The structural analysis of bacteriorhodopsin trapped in the M photointermediate state (1), the structures in the oxidized and reduced forms of cytochromes c 3 that perform a coupled two-electron step associated with proton transfer (2, 3), and the establishment of the coupled transfer of electrons and protons to the 3Fe-4S cluster of Azotobacter vinelandii ferredoxin (4) are just a few recent examples where results from different techniques are integrated in a description at the atomic level of the energy-transducing events. The phenomenon of energy transduction relies on coupled events (5), whether they involve only electrostatic interactions or structural rearrangements of the active sites or its surroundings (mechano-chemical coupling), which may be more important than the electrostatic component of the overall coupling (6). The pumping of proton(s) at the beginning of re-reduction of cytochrome c oxidase (7) can be described using a model in which the electrostatic attraction of electrons and protons is overcome (8), a situation that requires structural changes involving charged residues. Small proteins capable of performing energy transduction provide easier access to the structural bases for the underlying mechanisms, as the recent advances in the understanding of the proton pumping by the 26-kDa bacteriorhodopsin demonstrate (1, 9).This wo...

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Section: Discussionsupporting

confidence: 84%

Conformational Component in the Coupled Transfer of Multiple Electrons and Protons in a Monomeric Tetraheme Cytochrome

Louro¹,

Bento²,

Matías³

et al. 2001

Journal of Biological Chemistry

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“…Thus, HAO may be the agent that ameliorates the potential toxicity of hydroxylamine produced by a substrate-promiscuous (ammonia-oxidizing) pMMO of this and related type X and type I methanotrophs. We note that the Hao proteins of the non-aAOB lack N-and C-terminal regions, which are thought to be involved in docking for electron transfer to cytochrome c 554 (27) or membrane association in the vicinity of c m552 and ubiquinone. The putative absence of the electron transfer to ubiquinone would deprive the system of reductant for pMMO and force electrons (from hydroxylamine) to cytochrome oxidase, bypassing the proton motive force-generating cytochrome bc 1 complex.…”

Section: Resultsmentioning

confidence: 94%

“…The present work established for the first time a molecular evolutionary basis for the congruent heme stacking in HAO, cytochrome c nitrite reductase, and tetrathionate reductase. Despite conserved heme stacking, secondary and tertiary structure, HAO and cytochrome c 554 of Nitrosomonas (27,28) and the tetraheme portion of fumarate reductase (49) did not display high enough sequence similarity with Hao to justify their inclusion into a phylogenetic analysis. In marked contrast to the observed distribution of hao-orf2 gene tandems in aAOB and non-aAOB, cytochrome c 554 (cycA) has been found only in aAOB.…”

Section: Resultsmentioning

confidence: 99%

Structure and Sequence Conservation of hao Cluster Genes of Autotrophic Ammonia-Oxidizing Bacteria: Evidence for Their Evolutionary History

Bergmann

Hooper

Klotz

2005

Appl Environ Microbiol

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Comparison of the organization and sequence of the hao (hydroxylamine oxidoreductase) gene clusters from the gammaproteobacterial autotrophic ammonia-oxidizing bacterium (aAOB) Nitrosococcus oceani and the betaproteobacterial aAOB Nitrosospira multiformis and Nitrosomonas europaea revealed a highly conserved gene cluster encoding the following proteins: hao, hydroxylamine oxidoreductase; orf2, a putative protein; cycA, cytochrome c 554 ; and cycB, cytochrome c m552 . The deduced protein sequences of HAO, c 554 , and c m552 were highly similar in all aAOB despite their differences in species evolution and codon usage. Phylogenetic inference revealed a broad family of multi-c-heme proteins, including HAO, the pentaheme nitrite reductase, and tetrathionate reductase. The c-hemes of this group also have a nearly identical geometry of heme orientation, which has remained conserved during divergent evolution of function. High sequence similarity is also seen within a protein family, including cytochromes c m552 , NrfH/B, and NapC/NirT. It is proposed that the hydroxylamine oxidation pathway evolved from a nitrite reduction pathway involved in anaerobic respiration (denitrification) during the radiation of the Proteobacteria. Conservation of the hydroxylamine oxidation module was maintained by functional pressure, and the module expanded into two separate narrow taxa after a lateral gene transfer event between gamma-and betaproteobacterial ancestors of extant aAOB. HAOencoding genes were also found in six non-aAOB, either singly or tandemly arranged with an orf2 gene, whereas a c 554 gene was lacking. The conservation of the hao gene cluster in general and the uniqueness of the c 554 gene in particular make it a suitable target for the design of primers and probes useful for molecular ecology approaches to detect aAOB.

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“…Heme 2 is five coordinate with one axial His ligand. 16,17 The four hemes in cyt c 554 are present in two diheme pairs (hemes 2/4, hemes 1/3). Similar heme packing motifs have been observed in a family multiheme proteins, which includes hydroxylamine oxidoreductase (HAO), 18 cytochrome c nitrite reductase (NiR), 19, 20 fumarate reductase, 21 -23 NapB, 24 diheme cytochrome c ,25 and the split-Soret cytochrome.…”

Section: Introductionmentioning

confidence: 99%

NO Reductase Activity of the Tetraheme Cytochromec₅₅₄ofNitrosomonas europaea

2006

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The tetraheme cytochrome c 554 (cyt c 554 ) from Nitrosomonas europaea is believed to function as an electron-transfer protein from hydroxylamine oxidoreductase (HAO). We show here that cyt c 554 also has significant NO reductase activity. The protein contains one high-spin and three low-spin ctype hemes. HAO catalyzed reduction of the cyt c 554 , ligand binding, intermolecular electron transfer, and kinetics of NO reduction by cyt c 554 have been investigated. We detect the formation of a NObound ferrous heme species in cyt c 554 by EPR and Mössbauer spectroscopies during the HAO catalyzed oxidation of hydroxylamine, indicating that N-oxide intermediates produced from HAO readily bind to cyt c 554 . In the half-reduced state of cyt c 554 , we detect a spin interaction between the [FeNO] 7 state of heme 2 and the low-spin ferric state of heme 4. We find that ferrous cyt c 554 will reduce NO at a rate greater than 16 s −1 , which is comparable to rates of other known NO reductases. Carbon monoxide or nitrite are shown not to bind to the reduced protein, and previous results indicate the reactions with O 2 are slow and that a variety of ligands will not bind in the oxidized state. Thus, the enzymatic site is highly selective for NO. The NO reductase activity of cyt c 554 may be important during ammonia oxidation in N. europaea at low oxygen concentrations to detoxify NO produced by reduction of nitrite or incomplete oxidation of hydroxylamine.

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High-resolution structures of the oxidized and reduced states of cytochrome c554 from Nitrosomonas europaea

Cited by 50 publications

References 16 publications

Conformational Component in the Coupled Transfer of Multiple Electrons and Protons in a Monomeric Tetraheme Cytochrome

Conformational Component in the Coupled Transfer of Multiple Electrons and Protons in a Monomeric Tetraheme Cytochrome

Structure and Sequence Conservation of hao Cluster Genes of Autotrophic Ammonia-Oxidizing Bacteria: Evidence for Their Evolutionary History

NO Reductase Activity of the Tetraheme Cytochromec₅₅₄ofNitrosomonas europaea

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High-resolution structures of the oxidized and reduced states of cytochrome c554 from Nitrosomonas europaea

Cited by 50 publications

References 16 publications

Conformational Component in the Coupled Transfer of Multiple Electrons and Protons in a Monomeric Tetraheme Cytochrome

Conformational Component in the Coupled Transfer of Multiple Electrons and Protons in a Monomeric Tetraheme Cytochrome

Structure and Sequence Conservation of hao Cluster Genes of Autotrophic Ammonia-Oxidizing Bacteria: Evidence for Their Evolutionary History

NO Reductase Activity of the Tetraheme Cytochromec554ofNitrosomonas europaea

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NO Reductase Activity of the Tetraheme Cytochromec₅₅₄ofNitrosomonas europaea