Evolution of the soluble nitrate reductase: defining the monomeric periplasmic nitrate reductase subgroup

Jepson, Brian J. N.; Marietou, Angeliki; Mohan, Sudesh B.; Cole, Jeffrey A.; Butler, Catherine; Richardson, David J.

doi:10.1042/bst0340122

Cited by 48 publications

(44 citation statements)

References 26 publications

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“…These include E. coli, and the weak association of NapB with NapA in this organism may allow for some promiscuity of NapA in also accepting electrons via NapG. However, this would not be the case for the R. sphaeroides or the P. pantotrophus where the tight association between NapA and NapB precludes electron supply from diverse sources and in which, accordingly, napG is not present in the nap gene clusters (2,16,18).…”

Section: Resultsmentioning

confidence: 87%

“…In this evolutionary view the primordial "cytoplasmic" enzyme would have become fused to a signal peptide allowing it to be translocated to the periplasmic compartment where it would need a new electron donor to enable it to derive electrons from the respiratory electron transport chain. The monomeric NapA of the ␦-proteobacterium D. desulfuricans lies in a clade that includes the closest known NapA relatives of the assimilatory nitrate reductase and that do not interact with a NapB-type protein (16,17). During evolution, when NapA recruited the primordial NapB as a redox partner the molecular interaction would initially have been weak.…”

Section: Resultsmentioning

confidence: 99%

“…S2) and so may play an important role in NapAB interactions and electron transfer in both systems. It is then notable that it is absent in D. desulfuricans (17), Symbiobacterium thermophilum, and Desulfitobacterium hafniense NapA, all of which are thought to be NapB-independent enzymes (16). In analyzing the structure of heterodimeric NapAB from R. sphaeroides, Arnoux et al (10) used the D. desulfuricans monomeric NapA as a model to assess possible conformational changes between the monomeric and heterodimeric states and noted a 5°rigid body motion of domain IV between the heterodimeric R. sphaeroides and monomeric D. desulfuricans NapAs.…”

Section: Figure 3 Spectropotentiometric Properties Of the Momentioning

confidence: 99%

“…A 3.2-Å resolution structure of this enzyme suggests that tight complex formation is contributed to by two loops at the N-and C-terminal extremities of NapB that adopt an extended conformation and embrace the NapA subunit (10). However, another structure of NapA, the 1.9 Å resolution structure from the ␦-proteobacterium Desulfovibrio desulfuricans, is that of a monomer, and there is currently no evidence that this enzyme ever forms a heterodimer with a NapB subunit (9,16,17). This has led to a subclassification of periplasmic nitrate reductases into monomeric and heterodimeric members (10).…”

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confidence: 99%

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Spectropotentiometric and Structural Analysis of the Periplasmic Nitrate Reductase from Escherichia coli

Jepson¹,

Mohan

Clarke³

et al. 2007

Journal of Biological Chemistry

105

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The Escherichia coli NapA (periplasmic nitrate reductase) contains a [4Fe-4S] cluster and a Mo-bis-molybdopterin guanine dinucleotide cofactor. The NapA holoenzyme associates with a di-heme c-type cytochrome redox partner (NapB). These proteins have been purified and studied by spectropotentiometry, and the structure of NapA has been determined. In contrast to the well characterized heterodimeric NapAB systems of ␣-proteobacteria, such as Rhodobacter sphaeroides and Paracoccus pantotrophus, the ␥-proteobacterial E. coli NapA and NapB proteins purify independently and not as a tight heterodimeric complex. This relatively weak interaction is reflected in dissociation constants of 15 and 32 M determined for oxidized and reduced NapAB complexes, respectively. The surface electrostatic potential of E. coli NapA in the apparent NapB binding region is markedly less polar and anionic than that of the ␣-proteobacterial NapA, which may underlie the weaker binding of NapB. The molybdenum ion coordination sphere of E. coli NapA includes two molybdopterin guanine dinucleotide dithiolenes, a protein-derived cysteinyl ligand and an oxygen atom. The Mo-O bond length is 2.6 Å , which is indicative of a water ligand. The potential range over which the Mo 6؉ state is reduced to the Mo 5؉ state in either NapA (between ؉100 and ؊100 mV) or the NapAB complex (؊150 to ؊350 mV) is much lower than that reported for R. sphaeroides NapA (midpoint potential Mo 6؉/5؉ > ؉350 mV), and the form of the Mo 5؉ EPR signal is quite distinct. In E. coli NapA or NapAB, the Mo 5؉ state could not be further reduced to Mo 4؉. We then propose a catalytic cycle for E. coli NapA in which nitrate binds to the Mo 5؉ ion and where a stable des-oxo Mo 6؉ species may participate.Bacterial nitrate reductases are molybdoenzymes that catalyze the two-electron reduction of nitrate to nitrite. They can be classified into three groups according to their localization and function, namely membrane-bound respiratory, periplasmic respiratory, or cytoplasmic assimilatory enzymes (1, 2). Bacterial respiratory membrane-bound nitrate reductases, such as Escherichia coli NarGHI, are generally integral membrane protein complexes that have an active site on the cytoplasmic face of the membrane and couple quinol oxidation by nitrate to the generation of a transmembrane proton electrochemical gradient (2). The catalytic subunit, NarG, contains a Mo-bis-molybdopterin guanine dinucleotide (Mo-bis-MGD) 3 cofactor and a [4Fe-4S] cluster (3, 4). Periplasmic nitrate reductases (Nap) are also linked to quinol oxidation in respiratory electron transport chains, but do not conserve the free energy of the QH 2 -nitrate couple. Nitrate reduction via Nap can be coupled to energy conservation if the primary quinone reductase, for example NADH dehydrogenase or formate dehydrogenase, generates a proton electrochemical gradient. Thus Nap systems have a range of physiological functions that include the disposal of reducing equivalents during aerobic growth on reduced carbon substrates and anaerob...

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Section: Resultsmentioning

confidence: 87%

Section: Resultsmentioning

confidence: 99%

Section: Figure 3 Spectropotentiometric Properties Of the Momentioning

confidence: 99%

mentioning

confidence: 99%

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Spectropotentiometric and Structural Analysis of the Periplasmic Nitrate Reductase from Escherichia coli

Jepson¹,

Mohan

Clarke³

et al. 2007

Journal of Biological Chemistry

105

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“…NapAB interaction subgroup is widely accepted as a more evolved group, and monomeric NAP is the evolutionary link from NAS to NAP (Jepson et al, 2006). The Nap-a-1 of Shewanella forms a close cluster with those from Vibrio species, while the NAP-a-2 forms a relatively independent branch.…”

Section: Nap Systems Of Shewanella Piezotolerans Y Chen Et Almentioning

confidence: 99%

Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3

Chen

Wang

et al. 2010

The ISME Journal

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Most of the Shewanella species contain two periplasmic nitrate reductases (NAP-a and NAP-b), which is a unique feature of this genus. In the present study, the physiological function and evolutionary relationship of the two NAP systems were studied in the deep-sea bacterium Shewanella piezotolerans WP3. Both of the WP3 nap gene clusters: nap-a (napD1A1B1C) and nap-b (napD2A2B2) were shown to be involved in nitrate respiration. Phylogenetic analyses suggest that NAP-b originated earlier than NAP-a. Tetraheme cytochromes NapC and CymA were found to be the major electron deliver proteins, and CymA also served as a sole electron transporter towards nitrite reductase. Interestingly, a DnapA2 mutant with the single functional NAP-a system showed better growth than the wild-type strain, when grown in nitrate medium, and it had a selective advantage to the wild-type strain. On the basis of these results, we proposed the evolution direction of nitrate respiration system in Shewanella: from a single NAP-b to NAP-b and NAP-a both, followed by the evolution to a single NAP-a. Moreover, the data presented here will be very useful for the designed engineering of Shewanella for more efficient respiring capabilities for environmental bioremediation.

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Assembly ofMoco inMo/WEnzymes

Leimkühler

2017

Encyclopedia of Inorganic and Bioinorganic Chemistry

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The biosynthesis of the molybdenum cofactor (Moco) is ubiquitous and highly conserved in all organisms from bacteria to humans. In Moco, the molybdenum atom is coordinated to a dithiolene group present in the pterin‐based 6‐alkyl side chain of molybdopterin (MPT). In general, the biosynthesis of Moco can be divided into three steps in eukaryotes, and four steps in bacteria and archaea: (i) the starting point is the formation of the cPMP from 5′GTP, (ii) in the second step MPT is formed by the insertion of two sulfur molecules into cPMP, (iii) in the third step the molybdenum atom is inserted into MPT and Moco is formed, and (iv) additional modification of Moco occurs in bacteria and archaea in a fourth step by the attachment of nucleotides (CMP or GMP) to the phosphate group of MPT, forming the dinucleotide variants of Moco. Further, small differences exist in Moco formation among the different phyla. In higher eukaryotes Moco biosynthesis is located in different cellular compartments, many individual Moco biosynthesis proteins appear to have several cellular roles, and some proteins are shared between different biosynthetic pathways. Further, bacteria contain a large variety of more than 60 different molybdoenzymes being involved in specific, however, usually nonessential redox reactions. In contrast, in humans only four different molybdoenzymes have been identified, and a defect in Moco biosynthesis is lethal due to the loss of sulfite oxidase activity. This review will focus on the biosynthesis of Moco in bacteria and humans.

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Evolution of the soluble nitrate reductase: defining the monomeric periplasmic nitrate reductase subgroup

Cited by 48 publications

References 26 publications

Spectropotentiometric and Structural Analysis of the Periplasmic Nitrate Reductase from Escherichia coli

Spectropotentiometric and Structural Analysis of the Periplasmic Nitrate Reductase from Escherichia coli

Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3

Assembly ofMoco inMo/WEnzymes

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