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

Fisher, Oriana S.; Kenney, Grace E.; Ross, Matthew O.; Ro, Soo Y.; Lemma, Betelehem E.; Batelu, Sharon; Thomas, Paul M.; Sosnowski, Victoria; DeHart, Caroline J.; Kelleher, Neil L.; Stemmler, Timothy L.; Hoffman, Brian M.; Rosenzweig, Amy C.

doi:10.1038/s41467-018-06681-5

Cited by 54 publications

(99 citation statements)

References 59 publications

(78 reference statements)

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“…pMMO, the central metabolic enzyme in methanotrophs, comprises three subunits, PmoC, PmoA, and PmoB, arranged in a trimer of PmoCAB protomers (16 -19). In most ␣-proteobacterial methanotrophs, the pmo operons encoding these three subunits contain up to four additional genes encoding the proteins PmoD, CopC, and CopD and a PCu A C domain (9,20,21). In the methanotroph Methylosinus trichosporium OB3b, these four genes are coregulated with the pmoC, pmoA, and pmoB genes, exhibiting mild up-regulation in response to copper (21).…”

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confidence: 99%

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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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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“…The gene is present in all bacteria encoding AMO or pMMO for ammonia/methane oxidation, sometimes as part of the xmo operon and sometimes elsewhere in the genome. However, homologues are not found in the genomes of the actinobacteria Mycobacteria and Nocardiodes that encode n-alkane targeting CuMMOs (9). This suggests that the Rhodoferax/Polaromonas CuMMOs identified in our study are functionally more similar to the better known proteobacterial pMMO/AMO enzymes than to the actinobacterial CuMMOs, a proposition supported by phylogenetic analysis, which places the actinobacterial CuMMOs well apart from all proteobacterial CuMMOs (Figure 1).…”

Section: Transcription Of Xmoa In Tailings Pond Water Enriched With Pmentioning

confidence: 54%

“…A difference between the CuMMO-encoding genes in our Comomonadaceae versus those of Actinobacteria is the presence of xmoD in the former. The product of xmoD was recently described as a critical component of some CuMMOs: a Cucontaining polypeptide that may facilitate assembly and stabilization of the CuMMO complex, or facilitate electron delivery to the active site (9). The gene is present in all bacteria encoding AMO or pMMO for ammonia/methane oxidation, sometimes as part of the xmo operon and sometimes elsewhere in the genome.…”

Section: Transcription Of Xmoa In Tailings Pond Water Enriched With Pmentioning

confidence: 99%

Novel copper-containing membrane monooxygenases (CuMMOs) encoded by alkane-utilizing Betaproteobacteria

et al. 2019

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Copper-containing membrane monooxygenases (CuMMOs) are encoded by xmoCAB(D) gene clusters and catalyze the oxidation of methane, ammonia, or some short chain alkanes and alkenes. In a metagenome constructed from an oilsands tailings pond we detected an xmoCABD gene cluster with <59% derived amino acid identity to genes from known bacteria. Stable isotope probing experiments combined with a specific xmoA qPCR assay demonstrated that the bacteria possessing these genes were incapable of methane assimilation, but did grow on ethane and propane. Single-cell genomes (SAGs) from propane-enriched samples were therefore constructed and screened with the specific PCR assay to identify bacteria possessing the target gene cluster. Multiple SAGs of Betaproteobacteria belonging to the genera Rhodoferax and Polaromonas possessed close homologues of the metagenomic xmoCABD gene cluster. Unexpectedly, each of these two genera also possessed other xmoCABD paralogs, representing two additional lineages in phylogenetic analyses. Metabolic reconstructions from SAGs predicted that neither bacterium was capable of catabolic methane or ammonia oxidation, but that both were capable of higher nalkane degradation. The involvement of the encoded CuMMOs in alkane oxidation was further suggested by reverse transcription PCR analyses, which detected elevated transcription of the xmoA genes upon enrichment of water samples with propane as the sole energy source. Enrichments, isotope incorporation studies, genome reconstructions, and gene expression studies therefore all agreed that the unknown xmoCABD operons did not encode methane or ammonia monooxygenases, but rather n-alkane monooxygenases. This study broadens the known diversity of CuMMOs and identifies non-nitrifying Betaproteobacteria as possessing these enzymes.

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“…Também pode ser empregada no fracionamento de substâncias húmicas em diferentes sistemas de cultivo e em diferentes matrizes, para determinar parâmetros moleculares como o raio hidrodinâmico e a comum massa molecular, a distribuição do peso molecular de metais nos extratos de biomassa de fungos ou extrair e separar com sucesso diferentes frações de peso molecular de diferentes matrizes. [68][69][70][71][72][73][74][75][76] A cromatografia de exclusão por tamanho também pode ser acoplada a um espectrômetro de massa com plasma indutivamente acoplado, tornandose uma técnica eficiente de detecção e especiação de metaloproteínas ou metalobiomoléculas. 77 Como pode ser visto no trabalho de Lopes Júnior et al 77 em que buscaram avaliar a influência do cádmio no metabolismo do girassol, os autores utilizaram a SEC-ICP-MS para detectar a presença de metalobiomoléculas nas sementes de girassol e observaram que esse metal se ligava normalmente a compostos de massas moleculares de 3 a 70 kDa.…”

Section: Cromatografia Por Exclusão De Tamanhosunclassified

Metallomics: Methodologies and Applications in Environmental Studies

Silva¹,

Silva²

2020

Rev. Virtual Quim.

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Metallomics is an interdisciplinary area that has grown in recent years thanks to the development and application of techniques such as electrophoresis, chromatography, and spectrometry. Advances in this area, have allowed studies of functional and structural characterization of proteins linked to metals in different organisms and tissues, and thus, led to the understanding of the complex processes involving metalloproteins, and with this, their application for the realization of environmental monitoring studies. In this article, a review of the main metallomic techniques and their applications in environmental studies was carried out from 2008 to 2018, based on the search for scientific articles in the "Scopus" database. A metalômica é uma área interdisciplinar que tem crescido nos últimos anos, em virtude ao desenvolvimento e aplicação de técnicas como eletroforese, cromatografia e espectrometria. Avanços nessa área, têm permitido estudos de caracterização funcional e estrutural de proteínas ligadas a metais em diferentes organismos e tecidos, e desta forma, levado à compreensão, dos complexos processos que envolvem as metaloproteínas, e com isto, garantido sua aplicação para a realização de estudos de monitoramento ambiental. No presente artigo, foi realizada uma revisão das principais técnicas metalômicas e de suas aplicações em estudos ambientais no período de 2008 a 2018, a partir da busca de artigos científicos na base de dados "Scopus".

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

Cited by 54 publications

References 59 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

Novel copper-containing membrane monooxygenases (CuMMOs) encoded by alkane-utilizing Betaproteobacteria

Metallomics: Methodologies and Applications in Environmental Studies

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