From micelles to bicelles: Effect of the membrane on particulate methane monooxygenase activity

Ro, Soo Y.; Ross, Matthew O.; Deng, Yue Wen; Batelu, Sharon; Lawton, Thomas J.; Hurley, Joseph D.; Stemmler, Timothy L.; Hoffman, Brian M.; Rosenzweig, Amy C.

doi:10.1074/jbc.ra118.003348

Cited by 53 publications

(118 citation statements)

References 55 publications

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“…The histidine brace coordination geometry has been proposed to facilitate the formation of highvalent copper-oxygen intermediates for oxidation of an unactivated C-H bond in the substrate (26). Although the same effect has been proposed for the Cu B site in pMMO (26), which has similar coordination, albeit with a third histidine (18,19,38), recent work suggests that methane oxidation does not occur at this site (38).…”

Section: Pcu a C Domains Bind Copper Using A Histidine Bracementioning

confidence: 94%

PCuAC domains from methane-oxidizing bacteria use a histidine brace to bind copper

Fisher¹,

Sendzik

Ross

et al. 2019

Journal of Biological Chemistry

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Edited by Ruma Banerjee Copper is critically important for methanotrophic bacteria because their primary metabolic enzyme, particulate methane monooxygenase (pMMO), is copper-dependent. In addition to pMMO, many other copper proteins are encoded in the genomes of methanotrophs, including proteins that contain periplasmic copper-A chaperone (PCu A C) domains. Using bioinformatics analyses, we identified three distinct classes of PCu A C domain-containing proteins in methanotrophs, termed PmoF1, PmoF2, and PmoF3. PCu A C domains from other types of bacteria bind a single Cu(I) ion via an HX n MX 21/22 HXM motif, which is also present in PmoF3, but PmoF1 and PmoF2 lack this motif entirely. Instead, the PCu A C domains of PmoF1 and PmoF2 bind only Cu(II), and PmoF1 binds additional Cu(II) ions in a His-rich extension to its PCu A C domain. Crystal structures of the PmoF1 and PmoF2 PCu A C domains reveal that Cu(II) is coordinated by an N-terminal histidine brace HX 10 H motif. This binding site is distinct from those of previously characterized PCu A C domains but resembles copper centers in CopC proteins and lytic polysaccharide monooxygenase (LPMO) enzymes. Bioinformatics analysis of the entire PCu A C family reveals previously unappreciated diversity, including sequences that contain both the HX n MX 21/22 HXM and HX 10 H motifs, and sequences that lack either set of copper-binding ligands. These findings provide the first characterization of an additional class of copper proteins from methanotrophs, further expand the PCu A C family, and afford new insight into the biological significance of histidine bracemediated copper coordination. Copper enzymes, including cytochrome c oxidase, nitrous oxide reductase, nitrite reductase, superoxide dismutase, and particulate methane monooxygenase (pMMO), 4 play important roles in bacterial metabolism (1). In Gram-negative bacteria, these enzymes are located in the inner membrane and/or periplasm, where copper loading likely takes place via periplasmic chaperone proteins or directly from extracytoplasmic pools (2). One family of periplasmic copper-binding proteins implicated in assembly of the cytochrome c oxidase copper centers is the periplasmic copper-A chaperone (PCu A C) proteins. These proteins have been proposed to play a role in loading the cytochrome c oxidase Cu A and/or Cu B sites (3-8). Genes encoding PCu A Cs are often found neighboring genes encoding Sco1 proteins (3, 9), and transfer of Cu(I) from PCu A C to Sco1 has been demonstrated for PCu A Cs from Streptomyces lividans (7) and Rhodobacter capsulatus (10). However, it remains unclear whether PCu A C is absolutely required for metalation of cytochrome c oxidase because multiple gene disruption studies indicate that it is not critical for cytochrome c oxidase activity (5, 7, 11). In addition, there is evidence that some PCu A C homologs have other functions. For example, the PCu A C homolog AccA is essential for copper nitrite reductase activity in pathogenic Neisseria strains (12). Consistent with a broader ...

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Section: Pcu a C Domains Bind Copper Using A Histidine Bracementioning

confidence: 94%

PCuAC domains from methane-oxidizing bacteria use a histidine brace to bind copper

Fisher¹,

Sendzik

Ross

et al. 2019

Journal of Biological Chemistry

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“…To purify pMMO 48 , 51 , 52 , frozen cells were thawed in a lysis buffer consisting of 25 mM PIPES, pH 7.2 and 250 mM NaCl, except for Methylomicrobium alcaliphilum 20Z which required an alternate lysis buffer consisting of 25 mM PIPES, pH 7.2 and 500 mM NaCl. Cells were lysed via sonication, and cell debris was removed via centrifugation at 12,000 × g for 1 h at 4 °C.…”

Section: Methodsmentioning

confidence: 99%

Characterization of a long overlooked copper protein from methane- and ammonia-oxidizing bacteria

et al. 2018

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Methane-oxidizing microbes catalyze the oxidation of the greenhouse gas methane using the copper-dependent enzyme particulate methane monooxygenase (pMMO). Isolated pMMO exhibits lower activity than whole cells, however, suggesting that additional components may be required. A pMMO homolog, ammonia monooxygenase (AMO), converts ammonia to hydroxylamine in ammonia-oxidizing bacteria (AOB) which produce another potent greenhouse gas, nitrous oxide. Here we show that PmoD, a protein encoded within many pmo operons that is homologous to the AmoD proteins encoded within AOB amo operons, forms a copper center that exhibits the features of a well-defined CuA site using a previously unobserved ligand set derived from a cupredoxin homodimer. PmoD is critical for copper-dependent growth on methane, and genetic analyses strongly support a role directly related to pMMO and AMO. These findings identify a copper-binding protein that may represent a missing link in the function of enzymes critical to the global carbon and nitrogen cycles.

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“…Furthermore, a very recent EXAFS and EPR study has backed-up the findings from the quantum crystallographic work. 52 With the weight of evidence now swinging away from a dinuclear active site within pMMO and with the discovery of the histidine brace in LPMOs, there are major repercussions for our understanding of the mechanism of O2 activation and substrate oxidation at monomeric copper sites. Moreover, given that the C H bonds which both LPMOs and pMMOs oxidise are strong and unactivated, the postulate of a histidine brace coordinating a single copper is inspiring coordination chemists interested in preparing synthetic copper complexes which themselves could then be used as powerful oxidation catalysts.…”

Section: The Structure Of the Copper Histidine Brace In Pmmomentioning

confidence: 99%

Bracing copper for the catalytic oxidation of C–H bonds

et al. 2018

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A structural unit found in the active site of some copper proteins, the histidine brace is comprised of an N-terminal histidine which chelates a single copper ion through its amino terminus NH2 and the -N of its imidazole side chain, and coordination by the -N of a further histidine side chain, to give an overall N3 T-shaped coordination at the copper. The histidine brace appears in several proteins, including lytic polysaccharide monooxygenases (L)PMOs and particulate methane monooxygenases pMMOs, both of which catalyse the oxidation of substrates with strong C H bonds (bond dissociation enthalpies ~ 100 kcal/mol). As such, the copper histidine brace is the focus of research aimed at understanding how Nature catalyses the oxidation of unactivated C H bonds. In this Perspective, we evaluate these studies, which further give bioinspired direction to coordination chemists in the design and preparation of small molecule copper oxidation catalysts.

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From micelles to bicelles: Effect of the membrane on particulate methane monooxygenase activity

Cited by 53 publications

References 55 publications

PCuAC domains from methane-oxidizing bacteria use a histidine brace to bind copper

PCuAC domains from methane-oxidizing bacteria use a histidine brace to bind copper

Characterization of a long overlooked copper protein from methane- and ammonia-oxidizing bacteria

Bracing copper for the catalytic oxidation of C–H bonds

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