Structural basis of [NiFe] hydrogenase maturation by Hyp proteins

Watanabe, Satoshi; Sasaki, Daisuke; Tominaga, Taiga; Miki, Kunio

doi:10.1515/hsz-2012-0197

Cited by 34 publications

(37 citation statements)

References 57 publications

(80 reference statements)

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“…HypD proteins are approximately 40 kDa in size and contain a unique C-terminal CX 14 CX 6 CX 16 C motif in domain III that coordinates a [4Fe-4S] cluster, whereas domains I and II are both characterized as Rossmann folds [194,199,200]. The cluster environment in domain III shares similarities with the ferredoxin:thioredoxin reductase system wherein a redox cascade is created that involves the [4Fe-4S] cluster and a pair of cysteine residues that are in close proximity to it, although these Cys residues are not absolutely conserved in all HypD isoforms [197,199,201]. The redox cascade is extended to four other conserved motifs in HypD (CGXHXH, GPGCPVCX 2 P, GFETT, and PXHVSX 3 G) and this conduit has been proposed to play a role in the mechanism of iron cyanation [195,196,199].…”

Section: Fe(cn) 2 Co Cofactor Biosynthesis: Hypc and Hypdmentioning

confidence: 99%

“…HypA coordinates a single Ni 2+ ion with micromolar affinity via an Nterminal MHE motif [208][209][210], and also binds Zn 2+ through the cysteine thiolates of a zinc finger motif [208]. While the Ni 2+ and Zn 2+ binding domains are independent of one another, the presence of Ni 2+ appears to help dictate the orientation of these two domains, likely as a mechanism to mediate protein-protein interactions [201,208,210]. Moreover, HypA exhibits low sequence conservation outside of the Ni 2+ and Zn 2+ motifs; this mirrors the sequence diversity in both HypB and [NiFe]-hydrogenase, all three of which putatively interact during Ni 2+ delivery [201].…”

Section: Insertion Of Ni 2+ : Hypa and Hypbmentioning

confidence: 99%

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[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation

Peters

Schut

Boyd

et al. 2015

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

423

397

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The [FeFe]- and [NiFe]-hydrogenases catalyze the formal interconversion between hydrogen and protons and electrons, possess characteristic non-protein ligands at their catalytic sites and thus share common mechanistic features. Despite the similarities between these two types of hydrogenases, they clearly have distinct evolutionary origins and likely emerged from different selective pressures. [FeFe]-hydrogenases are widely distributed in fermentative anaerobic microorganisms and likely evolved under selective pressure to couple hydrogen production to the recycling of electron carriers that accumulate during anaerobic metabolism. In contrast, many [NiFe]-hydrogenases catalyze hydrogen oxidation as part of energy metabolism and were likely key enzymes in early life and arguably represent the predecessors of modern respiratory metabolism. Although the reversible combination of protons and electrons to generate hydrogen gas is the simplest of chemical reactions, the [FeFe]- and [NiFe]-hydrogenases have distinct mechanisms and differ in the fundamental chemistry associated with proton transfer and control of electron flow that also help to define catalytic bias. A unifying feature of these enzymes is that hydrogen activation itself has been restricted to one solution involving diatomic ligands (carbon monoxide and cyanide) bound to an Fe ion. On the other hand, and quite remarkably, the biosynthetic mechanisms to produce these ligands are exclusive to each type of enzyme. Furthermore, these mechanisms represent two independent solutions to the formation of complex bioinorganic active sites for catalyzing the simplest of chemical reactions, reversible hydrogen oxidation. As such, the [FeFe]- and [NiFe]-hydrogenases are arguably the most profound case of convergent evolution. This article is part of a Special Issue entitled: Fe/S proteins: Analysis, structure, function, biogenesis and diseases.

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Section: Fe(cn) 2 Co Cofactor Biosynthesis: Hypc and Hypdmentioning

confidence: 99%

Section: Insertion Of Ni 2+ : Hypa and Hypbmentioning

confidence: 99%

[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation

Peters

Schut

Boyd

et al. 2015

Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

423

397

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“…The Ni atom in the NiFe(CN) 2 CO cofactor is bound to four thiolate groups, two of which also bridge the Fe(CN) 2 CO group (4,5). NiFe(CN) 2 CO biosynthesis requires specific maturation machinery, in which six Hyp proteins (HypA-HypF) play key roles (6,7). Four Hyp proteins (HypC-HypF) are involved in the biosynthesis and incorporation of the Fe(CN) 2 CO group (8)(9)(10)(11)(12)(13)(14)(15).…”

mentioning

confidence: 99%

Structural basis of a Ni acquisition cycle for [NiFe] hydrogenase by Ni-metallochaperone HypA and its enhancer

Watanabe

Kawashima

Nishitani

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The Ni atom at the catalytic center of [NiFe] hydrogenases is incorporated by a Ni-metallochaperone, HypA, and a GTPase/ATPase, HypB. We report the crystal structures of the transient complex formed between HypA and ATPase-type HypB (HypB AT ) with Ni ions. Transient association between HypA and HypB AT is controlled by the ATP hydrolysis cycle of HypB AT, which is accelerated by HypA. Only the ATP-bound form of HypB AT can interact with HypA and induces drastic conformational changes of HypA. Consequently, upon complex formation, a conserved His residue of HypA comes close to the N-terminal conserved motif of HypA and forms a Ni-binding site, to which a Ni ion is bound with a nearly square-planar geometry. The Ni binding site in the HypAB AT complex has a nanomolar affinity (K d = 7 nM), which is in contrast to the micromolar affinity (K d = 4 μM) observed with the isolated HypA. The ATP hydrolysis and Ni binding cause conformational changes of HypB AT , affecting its association with HypA. These findings indicate that HypA and HypB AT constitute an ATP-dependent Ni acquisition cycle for [NiFe]-hydrogenase maturation, wherein HypB AT functions as a metallochaperone enhancer and considerably increases the Ni-binding affinity of HypA.X-ray crystallography | metalloprotein | transient complex | metallochaperone A pproximately one-half of all cellular proteins require specific metal ions for proper function, which are delivered by specific metallochaperones (1, 2). However, the mechanisms of correct acquisition and delivery to target proteins of many metallochaperones remain poorly understood.[NiFe] hydrogenases harbor a complex metal cofactor, NiFe(CN) 2 CO, in their active sites (3). This cofactor catalyzes reversible H 2 production. The Ni atom in the NiFe(CN) 2 CO cofactor is bound to four thiolate groups, two of which also bridge the Fe(CN) 2 CO group (4, 5). NiFe(CN) 2 CO biosynthesis requires specific maturation machinery, in which six Hyp proteins (HypA-HypF) play key roles (6, 7). Four Hyp proteins (HypC-HypF) are involved in the biosynthesis and incorporation of the Fe(CN) 2 CO group (8-15). After Fe insertion, HypA and HypB insert the Ni ion into the hydrogenase large subunit (16).HypA is a Ni-metallochaperone that binds to a Ni ion with micromolar affinity (17-19), and its structure consists of a Ni-binding domain (NiBD) and a Zn-binding domain (ZnBD) (20, 21). The NiBD contains a highly conserved MHE motif that is essential for Ni binding at the N terminus (20,22). HypB consists of a common GTPase domain and a less conserved metal-binding region (23)(24)(25). Recently, ATPase-type HypB (HypB AT , previously abbreviated as mmHypB) proteins were identified from Thermococcales (26). GTPase and ATPase types of HypB belong to the SIMIBI class NTPase family and share a similar architecture, despite their low sequence similarity (27). HypA and HypB form a transient complex in the Ni insertion process (17,22,28,29). In the Escherichia coli system, Ni transfer occurs from HypB to HypA (30). However, the functi...

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“…SIMIBI NTPases, but belong to the G3E family and carry the signature motif (ESGG) and the guanine specificity loop (NKTD) characteristic for this family (29,38). In contrast to AcsF Ch , they act together with other maturation factors to transfer a metal to a target protein: UreG forms a complex with the additional factors UreD (UreH), UreE and UreF to facilitate apo-urease maturation (8,39,40), whereas HypB is believed to process and deliver Ni 2ϩ in cooperation with HypA and SlyD to the large subunit of Ni,Fe-hydrogenase (7,10,41,42). In contrast, AcsF Ch is able to mature apo-ACS in vitro without additional proteins required.…”

Section: Nickelmentioning

confidence: 99%

“…How metalloenzymes mature has been investigated for some systems, revealing surprisingly complex maturation pathways (2)(3)(4)(5)(6)(7)(8). Enzymes containing nickel, although still relatively small in number, play critical roles in archaea, bacteria, and eukarya, through which they impact the global hydrogen (Ni,Fe-hydrogenase), nitrogen (urease), and carbon (acetylCoA synthase, carbon monoxide dehydrogenase, and methylCoM reductase) cycles (9).…”

mentioning

confidence: 99%

AcsF Catalyzes the ATP-dependent Insertion of Nickel into the Ni,Ni-[4Fe4S] Cluster of Acetyl-CoA Synthase

Gregg

Goetzl

Jeoung

et al. 2016

Journal of Biological Chemistry

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Acetyl-CoA synthase (ACS) catalyzes the reversible condensation of CO, CoA, and a methyl-cation to form acetyl-CoA at a unique Ni,Ni-[4Fe4S] cluster (the A-cluster). However, it was unknown which proteins support the assembly of the A-cluster. We analyzed the product of a gene from the cluster containing the ACS gene, cooC2 from Carboxydothermus hydrogenoformans, named AcsF Ch , and showed that it acts as a maturation factor of ACS. AcsF Ch and inactive ACS form a stable 2:1 complex that binds two nickel ions with higher affinity than the individual components. The nickel-bound ACS-AcsF Ch complex remains inactive until MgATP is added, thereby converting inactive to active ACS. AcsF Ch is a MinD-type ATPase and belongs to the CooC protein family, which can be divided into homologous subgroups. We propose that proteins of one subgroup are responsible for assembling the Ni,Ni-[4Fe4S] cluster of ACS, whereas proteins of a second subgroup mature the [Ni4Fe4S] cluster of carbon monoxide dehydrogenases.The cellular maturation of metalloenzymes, previously considered a spontaneous process in vivo, typically depends on a machinery of uptake, storage, processing, and delivery factors (1). How metalloenzymes mature has been investigated for some systems, revealing surprisingly complex maturation pathways (2-8). Enzymes containing nickel, although still relatively small in number, play critical roles in archaea, bacteria, and eukarya, through which they impact the global hydrogen (Ni,Fe-hydrogenase), nitrogen (urease), and carbon (acetylCoA synthase, carbon monoxide dehydrogenase, and methylCoM reductase) cycles (9). For most of these enzymes, we now have a good understanding of how nickel is incorporated into the active site (8, 10).The nickel-enzymes acetyl-CoA synthase (ACS) 2 and carbon monoxide dehydrogenase (CODH) are found in a variety of anaerobic microbes, including bacterial sulfate reducers, acetogens, and hydrogenogens, as well as archaeal methanogens and sulfate reducers, where they act as the prime CO 2 and CO converter (11)(12)(13)(14). ACS and CODH can be found as independent monofunctional enzymes in Carboxydothermus hydrogenoformans (15) but are typically found in other microorganisms as protein complexes: in acetogens ACS and CODH form a bifunctional (␣␤) 2 complex, whereas in methanogens they are part of a large (␣␤␥␦⑀) 8 multienzyme complex (11,13,15,16). CODHs catalyze the reversible reduction of CO 2 to CO at the C-cluster, in which a single nickel ion, embedded within a 3Fe-4S scaffold with an additional iron in exo, binds and activates CO and CO 2 for turnover (17)(18)(19). ACS catalyzes the reversible condensation of CO, CoA, and a methyl-cation donated by the methylated corrinoid iron-sulfur protein to form acetyl-CoA (13). ACS depends on a Ni,Ni-[4Fe4S] cluster (also called A-cluster) for activity, in which the two nickel ions have distinct coordinations: the nickel ion distal to the [4Fe4S] cluster (Ni d ) is coordinated by two amide nitrogen atoms and two cysteine thiolates within a Cys-X-Cys ...

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Structural basis of [NiFe] hydrogenase maturation by Hyp proteins

Cited by 34 publications

References 57 publications

[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation

[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation

Structural basis of a Ni acquisition cycle for [NiFe] hydrogenase by Ni-metallochaperone HypA and its enhancer

AcsF Catalyzes the ATP-dependent Insertion of Nickel into the Ni,Ni-[4Fe4S] Cluster of Acetyl-CoA Synthase

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