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Orchestrating copper binding: structure and variations on the cupredoxin fold

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Abstract

A large number of copper binding proteins coordinate metal ions using a shared three-dimensional fold called the cupredoxin domain. This domain was originally identified in Type 1 “blue copper” centers but has since proven to be a common domain architecture within an increasingly large and diverse group of copper binding domains. The cupredoxin fold has a number of qualities that make it ideal for coordinating Cu ions for purposes including electron transfer, enzyme catalysis, assembly of other copper sites, and copper sequestration. The structural core does not undergo major conformational changes upon metal binding, but variations within the coordination environment of the metal site confer a range of Cu-binding affinities, reduction potentials, and spectroscopic properties. Here, we discuss these proteins from a structural perspective, examining how variations within the overall cupredoxin fold and metal binding sites are linked to distinct spectroscopic properties and biological functions. Expanding far beyond the blue copper proteins, cupredoxin domains are used by a growing number of proteins and enzymes as a means of binding copper ions, with many more likely remaining to be identified.

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References

  1. Decaria L, Bertini I, Williams RJP (2011) Copper proteomes, phylogenetics and evolution. Metallomics 3:56–60. https://doi.org/10.1039/c0mt00045k

    Article  CAS  PubMed  Google Scholar 

  2. Andreini C, Banci L, Bertini I, Rosato A (2008) Occurrence of copper proteins through the three domains of life: a bioinformatic approach. J Proteome Res 7:209–216. https://doi.org/10.1021/pr070480u

    Article  CAS  PubMed  Google Scholar 

  3. Zaballa M-E, Abriata LA, Donaire A, Vila AJ (2012) Flexibility of the metal-binding region in apo-cupredoxins. Proc Natl Acad Sci USA 109:9254–9259. https://doi.org/10.1073/pnas.1119460109

    Article  PubMed  PubMed Central  Google Scholar 

  4. Colman PM, Freeman HC, Guss JM et al (1978) X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution. Nature 272:319–324. https://doi.org/10.1038/272319a0

    Article  CAS  Google Scholar 

  5. Richardson JS, Richardson DC, Thomas KA et al (1976) Similarity of three-dimensional structure between the immunoglobulin domain and the copper, zinc superoxide dismutase subunit. J Mol Biol 102:221–235. https://doi.org/10.1016/S0022-2836(76)80050-2

    Article  CAS  PubMed  Google Scholar 

  6. Adman ET (1991) Copper protein structures. Adv Protein Chem 42:145–197. https://doi.org/10.1016/s0065-3233(08)60536-7

    Article  CAS  PubMed  Google Scholar 

  7. El-Gebali S, Mistry J, Bateman A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995

    Article  CAS  PubMed  Google Scholar 

  8. Dennison C (2005) Investigating the structure and function of cupredoxins. Coord Chem Rev 249:3025–3054. https://doi.org/10.1016/j.ccr.2005.04.021

    Article  CAS  Google Scholar 

  9. Savelieff MG, Wilson TD, Elias Y et al (2008) Experimental evidence for a link among cupredoxins: red, blue, and purple copper transformations in nitrous oxide reductase. Proc Natl Acad Sci USA 105:7919–7924. https://doi.org/10.1073/pnas.0711316105

    Article  PubMed  PubMed Central  Google Scholar 

  10. Goyal A, Madan B, Lee K-SH (2015) Identification of novel cupredoxin homologs using overlapped conserved residues based approach. J Microbiol Biotechnol 25:127–136. https://doi.org/10.4014/jmb.1409.09021

    Article  CAS  PubMed  Google Scholar 

  11. Land M, Hauser L, Jun S-R et al (2015) Insights from 20 years of bacterial genome sequencing. Funct Integr Genomics 15:141–161. https://doi.org/10.1007/s10142-015-0433-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Murphy MEP, Lindley PF, Adman ET (1997) Structural comparison of cupredoxin domains: domain recycling to construct proteins with novel functions. Protein Sci 6:761–770. https://doi.org/10.1002/pro.5560060402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Dennison C (2008) The role of ligand-containing loops at copper sites in proteins. Nat Prod Rep 25:15–24. https://doi.org/10.1039/B707987G

    Article  CAS  PubMed  Google Scholar 

  14. Paltrinieri L, Borsari M, Battistuzzi G et al (2013) How the dynamics of the metal-binding loop region controls the acid transition in cupredoxins. Biochemistry 52:7397–7404. https://doi.org/10.1021/bi400860n

    Article  CAS  PubMed  Google Scholar 

  15. Malmström BG (1994) Rack-induced bonding in blue-copper proteins. Eur J Biochem 223:711–718. https://doi.org/10.1111/j.1432-1033.1994.tb19044.x

    Article  PubMed  Google Scholar 

  16. Abriata LA, Vila AJ, Dal Peraro M (2014) Molecular dynamics simulations of apocupredoxins: insights into the formation and stabilization of copper sites under entatic control. J Biol Inorg Chem 19:565–575. https://doi.org/10.1007/s00775-014-1108-7

    Article  CAS  PubMed  Google Scholar 

  17. Fisher OS, Sendzik MR, Ross MO et al (2019) PCuAC domains from methane-oxidizing bacteria use a histidine brace to bind copper. J Biol Chem 294:16351–16363. https://doi.org/10.1074/jbc.RA119.010093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Damle MS, Singh AN, Peters SC et al (2021) The YcnI protein from Bacillus subtilis contains a copper-binding domain. J Biol Chem 297:101078. https://doi.org/10.1016/j.jbc.2021.101078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Udagedara SR, Wijekoon CJK, **ao Z et al (2019) The crystal structure of the CopC protein from Pseudomonas fluorescens reveals amended classifications for the CopC protein family. J Inorg Biochem 195:194–200. https://doi.org/10.1016/j.**orgbio.2019.03.007

    Article  CAS  PubMed  Google Scholar 

  20. Bertini I, Bryant DA, Ciurli S et al (2001) Backbone dynamics of plastocyanin in both oxidation states. J Biol Chem 276:47217–47226. https://doi.org/10.1074/jbc.M100304200

    Article  CAS  PubMed  Google Scholar 

  21. Koch M, Velarde M, Harrison MD et al (2005) Crystal structures of oxidized and reduced stellacyanin from horseradish roots. J Am Chem Soc 127:158–166. https://doi.org/10.1021/ja046184p

    Article  CAS  PubMed  Google Scholar 

  22. Gudmundsson M, Kim S, Wu M et al (2014) Structural and electronic snapshots during the transition from a Cu(II) to Cu(I) metal center of a lytic polysaccharide monooxygenase by X-ray photoreduction. J Biol Chem 289:18782–18792. https://doi.org/10.1074/jbc.M114.563494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Frandsen KEH, Simmons TJ, Dupree P et al (2016) The molecular basis of polysaccharide cleavage by lytic polysaccharide monooxygenases. Nat Chem Biol 12:298–303. https://doi.org/10.1038/nchembio.2029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hemsworth GR, Taylor EJ, Kim RQ et al (2013) The copper active site of CBM33 polysaccharide oxygenases. J Am Chem Soc 135:6069–6077. https://doi.org/10.1021/ja402106e

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Blundell KL, Hough MA, Vijgenboom E, Worrall JA (2014) Structural and mechanistic insights into an extracytoplasmic copper trafficking pathway in Streptomyces lividans. Biochem J 459:525–538. https://doi.org/10.1042/BJ20140017

    Article  CAS  PubMed  Google Scholar 

  26. Wijekoon CJK, Young TR, Wedd AG, **ao Z (2015) CopC protein from Pseudomonas fluorescens SBW25 features a conserved novel high-affinity Cu(II) binding site. Inorg Chem 54:2950–2959. https://doi.org/10.1021/acs.inorgchem.5b00031

    Article  CAS  PubMed  Google Scholar 

  27. Zhang L, Koay M, Maher MJ et al (2006) Intermolecular transfer of copper ions from the CopC protein of Pseudomonas syringae. Crystal structures of fully loaded CuI CuII forms. J Am Chem Soc 128:5834–5850. https://doi.org/10.1021/ja058528x

    Article  CAS  PubMed  Google Scholar 

  28. Fu Y, Bruce KE, Wu H, Giedroc DP (2016) The S2 Cu(I) site in CupA from Streptococcus pneumoniae is required for cellular copper resistance. Metallomics 8:61–70. https://doi.org/10.1039/c5mt00221d

    Article  CAS  PubMed  Google Scholar 

  29. Adman ET, Turley S, Bramson R et al (1989) A 2.0-Å structure of the blue copper protein (cupredoxin) from Alcaligenes faecalis S-6. J Biol Chem 264:87–99. https://doi.org/10.1016/S0021-9258(17)31227-9

    Article  CAS  PubMed  Google Scholar 

  30. Choi M, Davidson VL (2011) Cupredoxins—a study of how proteins may evolve to use metals for bioenergetic processes. Metallomics 3:140. https://doi.org/10.1039/c0mt00061b

    Article  CAS  PubMed  Google Scholar 

  31. Jones SM, Solomon EI (2015) Electron transfer and reaction mechanism of laccases. Cell Mol Life Sci 72:869–883. https://doi.org/10.1007/s00018-014-1826-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gräff M, Buchholz PCF, Le Roes-Hill M, Pleiss J (2020) Multicopper oxidases: modular structure, sequence space, and evolutionary relationships. Proteins 88:1329–1339. https://doi.org/10.1002/prot.25952

    Article  CAS  PubMed  Google Scholar 

  33. Hakulinen N, Rouvinen J (2015) Three-dimensional structures of laccases. Cell Mol Life Sci 72:857–868. https://doi.org/10.1007/s00018-014-1827-5

    Article  CAS  PubMed  Google Scholar 

  34. Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-Å resolution containing a full complement of coppers. J Biol Chem 277:37663–37669. https://doi.org/10.1074/jbc.M204571200

    Article  CAS  PubMed  Google Scholar 

  35. Enguita FJ, Martins LO, Henriques AO, Carrondo MA (2003) Crystal structure of a bacterial endospore coat component. A laccase with enhanced thermostability properties. J Biol Chem 278:19416–19425. https://doi.org/10.1074/jbc.M301251200

    Article  CAS  PubMed  Google Scholar 

  36. Rubino JT, Franz KJ (2012) Coordination chemistry of copper proteins: how nature handles a toxic cargo for essential function. J Inorg Biochem 107:129–143. https://doi.org/10.1016/j.**orgbio.2011.11.024

    Article  CAS  PubMed  Google Scholar 

  37. Worrall JAR, Machczynski MC, Keijser BJF et al (2006) Spectroscopic characterization of a high-potential lipo-cupredoxin found in Streptomyces coelicolor. J Am Chem Soc 128:14579–14589. https://doi.org/10.1021/ja064112n

    Article  CAS  PubMed  Google Scholar 

  38. LaCroix LB, Randall DW, Nersissian AM et al (1998) Spectroscopic and geometric variations in perturbed blue copper centers: electronic structures of stellacyanin and cucumber basic protein. J Am Chem Soc 120:9621–9631. https://doi.org/10.1021/ja980606b

    Article  CAS  Google Scholar 

  39. Hart PJ, Eisenberg D, Nersissian AM et al (1996) A missing link in cupredoxins: crystal structure of cucumber stellacyanin at 1.6 Å resolution. Protein Sci 5:2175–2183. https://doi.org/10.1002/pro.5560051104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Nar H, Messerschmidt A, Huber R et al (1991) Crystal structure analysis of oxidized Pseudomonas aeruginosa azurin at pH 5.5 and pH 9.0. A pH-induced conformational transition involves a peptide bond flip. J Mol Biol 221:765–772. https://doi.org/10.1016/0022-2836(91)80173-r

    Article  CAS  PubMed  Google Scholar 

  41. Nersissian AM, Valentine JS, Immoos C et al (1998) Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci 7:1915–1929. https://doi.org/10.1002/pro.5560070907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Schininà ME, Maritano S, Barra D et al (1996) Mavicyanin, a stellacyanin-like protein from zucchini peelings: primary structure and comparison with other cupredoxins. Biochim Biophys Acta 1297:28–32. https://doi.org/10.1016/0167-4838(96)00079-9

    Article  PubMed  Google Scholar 

  43. Olsson MH, Ryde U (1999) The influence of axial ligands on the reduction potential of blue copper proteins. J Biol Inorg Chem 4:654–663. https://doi.org/10.1007/s007750050389

    Article  CAS  PubMed  Google Scholar 

  44. Clark KM, Yu Y, van der Donk WA et al (2014) Modulating the copper–sulfur interaction in type 1 blue copper azurin by replacing Cys112 with nonproteinogenic homocysteine. Inorg Chem Front 1:153–158. https://doi.org/10.1039/C3QI00096F

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yanagisawa S, Banfield MJ, Dennison C (2006) The role of hydrogen bonding at the active site of a cupredoxin: the Phe114Pro azurin variant. Biochemistry 45:8812–8822. https://doi.org/10.1021/bi0606851

    Article  CAS  PubMed  Google Scholar 

  46. Marshall NM, Garner DK, Wilson TD et al (2009) Rationally tuning the reduction potential of a single cupredoxin beyond the natural range. Nature 462:113–116. https://doi.org/10.1038/nature08551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wijma HJ, MacPherson I, Alexandre M et al (2006) A rearranging ligand enables allosteric control of catalytic activity in copper-containing nitrite reductase. J Mol Biol 358:1081–1093. https://doi.org/10.1016/j.jmb.2006.02.042

    Article  CAS  PubMed  Google Scholar 

  48. Szuster J, Leguto AJ, Zitare UA et al (2022) Electrochemical characterization of an engineered red copper protein featuring an unprecedented entropic control of the reduction potential. Bioelectrochemistry 146:108095. https://doi.org/10.1016/j.bioelechem.2022.108095

    Article  CAS  PubMed  Google Scholar 

  49. Hosseinzadeh P, Lu Y (2016) Design and fine-tuning redox potentials of metalloproteins involved in electron transfer in bioenergetics. Biochim Biophys Acta (BBA) Bioenerg 1857:557–581. https://doi.org/10.1016/j.bbabio.2015.08.006

    Article  CAS  Google Scholar 

  50. Sukumar N, Chen Z, Ferrari D et al (2006) Crystal structure of an electron transfer complex between aromatic amine dehydrogenase and azurin from Alcaligenes faecalis. Biochemistry 45:13500–13510. https://doi.org/10.1021/bi0612972

    Article  CAS  PubMed  Google Scholar 

  51. Zhu Z, Cunane LM, Chen Z et al (1998) Molecular basis for interprotein complex-dependent effects on the redox properties of amicyanin. Biochemistry 37:17128–17136. https://doi.org/10.1021/bi9817919

    Article  CAS  PubMed  Google Scholar 

  52. Lieberman RL, Arciero DM, Hooper AB, Rosenzweig AC (2001) Crystal structure of a novel red copper protein from Nitrosomonas europaea. Biochemistry 40:5674–5681. https://doi.org/10.1021/bi0102611

    Article  CAS  PubMed  Google Scholar 

  53. Arnesano F, Banci L, Bertini I, Thompsett AR (2002) Solution structure of CopC: a cupredoxin-like protein involved in copper homeostasis. Structure 10:1337–1347

    Article  CAS  Google Scholar 

  54. Basumallick L, Sarangi R, DeBeer GS et al (2005) Spectroscopic and density functional studies of the red copper site in nitrosocyanin: role of the protein in determining active site geometric and electronic structure. J Am Chem Soc 127:3531–3544. https://doi.org/10.1021/ja044412+

    Article  CAS  PubMed  Google Scholar 

  55. Arciero DM, Pierce BS, Hendrich MP, Hooper AB (2002) Nitrosocyanin, a red cupredoxin-like protein from Nitrosomonas europaea. Biochemistry 41:1703–1709. https://doi.org/10.1021/bi015908w

    Article  CAS  PubMed  Google Scholar 

  56. Roger M, Biaso F, Castelle CJ et al (2014) Spectroscopic characterization of a green copper site in a single-domain cupredoxin. PLoS ONE 9:e98941. https://doi.org/10.1371/journal.pone.0098941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Durand A, Fouesnard M, Bourbon M-L et al (2021) A periplasmic cupredoxin with a green CuT1.5 center is involved in bacterial copper tolerance. Metallomics 13:mfab067. https://doi.org/10.1093/mtomcs/mfab067

    Article  PubMed  Google Scholar 

  58. LaCroix LB, Shadle SE, Wang Y et al (1996) Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding, and implications for the entatic/rack state. J Am Chem Soc 118:7755–7768. https://doi.org/10.1021/ja961217p

    Article  CAS  Google Scholar 

  59. Roger M, Sciara G, Biaso F et al (2017) Impact of copper ligand mutations on a cupredoxin with a green copper center. Biochim Biophys Acta (BBA) Bioenerg 1858:351–359. https://doi.org/10.1016/j.bbabio.2017.02.007

    Article  CAS  Google Scholar 

  60. Beinert H (1997) Copper A of cytochrome c oxidase, a novel, long-embattled, biological electron-transfer site. Eur J Biochem 245:521–532. https://doi.org/10.1111/j.1432-1033.1997.t01-1-00521.x

    Article  CAS  PubMed  Google Scholar 

  61. Kroneck PMH (2018) Walking the seven lines: binuclear copper A in cytochrome c oxidase and nitrous oxide reductase. J Biol Inorg Chem 23:27–39. https://doi.org/10.1007/s00775-017-1510-z

    Article  CAS  PubMed  Google Scholar 

  62. Morgada MN, Murgida DH, Vila AJ (2020) Purple mixed-valent copper A. Met Ions Life Sci. https://doi.org/10.1515/9783110589757-010

    Article  PubMed  Google Scholar 

  63. Williams PA, Blackburn NJ, Sanders D et al (1999) The CuA domain of Thermus thermophilus ba3-type cytochrome c oxidase at 1.6 A resolution. Nat Struct Biol 6:509–516. https://doi.org/10.1038/9274

    Article  CAS  PubMed  Google Scholar 

  64. Pomowski A, Zumft WG, Kroneck PMH, Einsle O (2011) N2O binding at a [4Cu:2S] copper–sulphur cluster in nitrous oxide reductase. Nature 477:234–237. https://doi.org/10.1038/nature10332

    Article  CAS  PubMed  Google Scholar 

  65. Zhang L, Bill E, Kroneck PMH, Einsle O (2020) Histidine-bated proton-coupled electron transfer to the CuA site of nitrous oxide reductase. J Am Chem Soc. https://doi.org/10.1021/jacs.0c10057

    Article  PubMed  PubMed Central  Google Scholar 

  66. Brown K, Tegoni M, Prudêncio M et al (2000) A novel type of catalytic copper cluster in nitrous oxide reductase. Nat Struct Biol 7:191–195. https://doi.org/10.1038/73288

    Article  CAS  PubMed  Google Scholar 

  67. Farrar JA, Lappalainen P, Zumft WG et al (1995) Spectroscopic and mutagenesis studies on the CuA centre from the cytochrome-c oxidase complex of Paracoccus denitrificans. Eur J Biochem 232:294–303. https://doi.org/10.1111/j.1432-1033.1995.tb20811.x

    Article  CAS  PubMed  Google Scholar 

  68. Fisher OS, Kenney GE, Ross MO et al (2018) Characterization of a long overlooked copper protein from methane- and ammonia-oxidizing bacteria. Nat Commun 9:4276. https://doi.org/10.1038/s41467-018-06681-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ross MO, Fisher OS, Morgada MN et al (2019) Formation and electronic structure of an atypical CuA site. J Am Chem Soc 141:4678–4686. https://doi.org/10.1021/jacs.8b13610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Fu Y, Tsui H-CT, Bruce KE et al (2013) A new structural paradigm in copper resistance in Streptococcus pneumoniae. Nat Chem Biol 9:177–183. https://doi.org/10.1038/nchembio.1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Banci L, Bertini I, Ciofi-Baffoni S et al (2005) A copper(I) protein possibly involved in the assembly of CuA center of bacterial cytochrome c oxidase. Proc Natl Acad Sci USA 102:3994–3999. https://doi.org/10.1073/pnas.0406150102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Abriata LA, Banci L, Bertini I et al (2008) Mechanism of CuA assembly. Nat Chem Biol 4:599–601. https://doi.org/10.1038/nchembio.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Canonica F, Klose D, Ledermann R et al (2019) Structural basis and mechanism for metallochaperone assisted assembly of the CuA center in cytochrome oxidase. Sci Adv 5:eaaw8478

    Article  CAS  Google Scholar 

  74. Arnesano F, Banci L, Bertini I et al (2003) A redox switch in CopC: an intriguing copper trafficking protein that binds copper(I) and copper(II) at different sites. Proc Natl Acad Sci USA 100:3814–3819. https://doi.org/10.1073/pnas.0636904100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lawton TJ, Kenney GE, Hurley JD, Rosenzweig AC (2016) The CopC family: structural and bioinformatic insights into a diverse group of periplasmic copper binding proteins. Biochemistry 55:2278–2290. https://doi.org/10.1021/acs.biochem.6b00175

    Article  CAS  PubMed  Google Scholar 

  76. Ipsen JØ, Hernández-Rollán C, Muderspach SJ et al (2021) Copper binding and reactivity at the histidine brace motif: insights from mutational analysis of the Pseudomonas fluorescens copper chaperone CopC. FEBS Lett. https://doi.org/10.1002/1873-3468.14092

    Article  PubMed  Google Scholar 

  77. Ipsen JØ, Hallas-Møller M, Brander S et al (2021) Lytic polysaccharide monooxygenases and other histidine-brace copper proteins: structure, oxygen activation and biotechnological applications. Biochem Soc Trans 49:531–540. https://doi.org/10.1042/BST20201031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Chaplin AK, Wilson MT, Hough MA et al (2016) Heterogeneity in the histidine-brace copper coordination sphere in auxiliary activity family 10 (AA10) lytic polysaccharide monooxygenases. J Biol Chem 291:12838–12850. https://doi.org/10.1074/jbc.M116.722447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Forsberg Z, Bissaro B, Gullesen J et al (2018) Structural determinants of bacterial lytic polysaccharide monooxygenase functionality. J Biol Chem 293:1397–1412. https://doi.org/10.1074/jbc.M117.817130

    Article  CAS  PubMed  Google Scholar 

  80. Vaaje-Kolstad G, Forsberg Z, Loose JS et al (2017) Structural diversity of lytic polysaccharide monooxygenases. Curr Opin Struct Biol 44:67–76. https://doi.org/10.1016/j.sbi.2016.12.012

    Article  CAS  PubMed  Google Scholar 

  81. Chiu E, Hijnen M, Bunker RD et al (2015) Structural basis for the enhancement of virulence by viral spindles and their in vivo crystallization. Proc Natl Acad Sci USA 112:3973–3978. https://doi.org/10.1073/pnas.1418798112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Koo CW, Tucci FJ, He Y, Rosenzweig AC (2022) Recovery of particulate methane monooxygenase structure and activity in a lipid bilayer. Science 375:1287–1291. https://doi.org/10.1126/science.abm3282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434:177–182. https://doi.org/10.1038/nature03311

    Article  CAS  PubMed  Google Scholar 

  84. Lawton TJ, Ham J, Sun T, Rosenzweig AC (2014) Structural conservation of the B subunit in the ammonia monooxygenase/particulate methane monooxygenase superfamily. Proteins 82:2263–2267. https://doi.org/10.1002/prot.24535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Tamburrini KC, Terrapon N, Lombard V et al (2021) Bioinformatic analysis of lytic polysaccharide monooxygenases reveals the pan-families occurrence of intrinsically disordered C-terminal extensions. Biomolecules 11:1632. https://doi.org/10.3390/biom11111632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Quinlan RJ, Sweeney MD, Lo Leggio L et al (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci 108:15079–15084. https://doi.org/10.1073/pnas.1105776108

    Article  PubMed  PubMed Central  Google Scholar 

  87. Vu VV, Ngo ST (2018) Copper active site in polysaccharide monooxygenases. Coord Chem Rev 368:134–157. https://doi.org/10.1016/j.ccr.2018.04.005

    Article  CAS  Google Scholar 

  88. Petrović DM, Bissaro B, Chylenski P et al (2018) Methylation of the N-terminal histidine protects a lytic polysaccharide monooxygenase from auto-oxidative inactivation. Protein Sci 27:1636–1650. https://doi.org/10.1002/pro.3451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Ross MO, MacMillan F, Wang J et al (2019) Particulate methane monooxygenase contains only mononuclear copper centers. Science (New York, NY) 364:566–570. https://doi.org/10.1126/science.aav2572

    Article  CAS  Google Scholar 

  90. Frandsen KEH, Tovborg M, Jørgensen CI et al (2019) Insights into an unusual auxiliary activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases. J Biol Chem 294:17117–17130. https://doi.org/10.1074/jbc.RA119.009223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Labourel A, Frandsen KEH, Zhang F et al (2020) A fungal family of lytic polysaccharide monooxygenase-like copper proteins. Nat Chem Biol. https://doi.org/10.1038/s41589-019-0438-8

    Article  PubMed  Google Scholar 

  92. Capaldi RA (1990) Structure and function of cytochrome c oxidase. Annu Rev Biochem 59:569–596. https://doi.org/10.1146/annurev.bi.59.070190.003033

    Article  CAS  PubMed  Google Scholar 

  93. Carreira C, Pauleta SR, Moura I (2017) The catalytic cycle of nitrous oxide reductase—the enzyme that catalyzes the last step of denitrification. J Inorg Biochem 177:423–434. https://doi.org/10.1016/j.**orgbio.2017.09.007

    Article  CAS  PubMed  Google Scholar 

  94. Cvetkovic A, Menon AL, Thorgersen MP et al (2010) Microbial metalloproteomes are largely uncharacterized. Nature 466:779–782. https://doi.org/10.1038/nature09265

    Article  CAS  PubMed  Google Scholar 

  95. Hagedoorn P-L (2015) Emerging strategies in metalloproteomics. In: Nriagu JO, Skaar EP (eds) Trace metals and infectious diseases. MIT Press, Cambridge, MA

    Google Scholar 

  96. Andreini C, Bertini I, Rosato A (2009) Metalloproteomes: a bioinformatic approach. Acc Chem Res 42:1471–1479. https://doi.org/10.1021/ar900015x

    Article  CAS  PubMed  Google Scholar 

  97. Zhang Y, Zheng J (2020) Bioinformatics of metalloproteins and metalloproteomes. Molecules 25:3366. https://doi.org/10.3390/molecules25153366

    Article  CAS  PubMed Central  Google Scholar 

  98. Adman ET, Jensen LH (1981) Structural features of azurin at 2.7 Å resolution. Isr J Chem 21:8–12. https://doi.org/10.1002/ijch.198100003

    Article  CAS  Google Scholar 

  99. Xu Q, Dunbrack RL Jr (2012) Assignment of protein sequences to existing domain and family classification systems: Pfam and the PDB. Bioinformatics 28:2763–2772. https://doi.org/10.1093/bioinformatics/bts533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

Partial financial support was received from National Science Foundation Award CHE-2137107 (O.S.F.) and a Lehigh University College of Arts and Sciences Undergraduate Research Grant (J.G.).

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  1. Department of Chemistry, Lehigh University, Bethlehem, PA, USA

    **g Guo & Oriana S. Fisher

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Guo, J., Fisher, O.S. Orchestrating copper binding: structure and variations on the cupredoxin fold. J Biol Inorg Chem 27, 529–540 (2022). https://doi.org/10.1007/s00775-022-01955-2

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