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Abstract

Methanobactins (Mbns) are ribosomally synthesized and posttranslationally modified peptide natural products released by methanotrophic bacteria under conditions of copper scarcity. Mbns bind Cu(I) with high affinity via nitrogen-containing heterocycles and thioamide groups installed on a precursor peptide, MbnA, by a core biosynthetic enzyme complex, MbnBC. Additional stabilizing modifications are enacted by other, less universal biosynthetic enzymes. Copper-loaded Mbn is imported into the cell by TonB-dependent transporters called MbnTs, and copper is mobilized by an unknown mechanism. The machinery to biosynthesize and transport Mbn is encoded in operons that are also found in the genomes of nonmethanotrophic bacteria. In this review, we provide an update on the state of the Mbn field, highlighting recent discoveries regarding Mbn structure, biosynthesis, and handling as well as the emerging roles of Mbns in the environment and their potential use as therapeutics.

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2024-11-20
2025-02-11
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Literature Cited

  1. 1.
    Andrews SC, Robinson AK, Rodríguez-Quiñones F. 2003.. Bacterial iron homeostasis. . FEMS Microbiol. Rev. 27::21537
    [Crossref] [Google Scholar]
  2. 2.
    Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, et al. 2013.. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. . Nat. Prod. Rep. 30::10860
    [Crossref] [Google Scholar]
  3. 3.
    Ayikpoe RS, Zhu L, Chen JY, Ting CP, van der Donk WA. 2023.. Macrocyclization and backbone rearrangement during RiPP biosynthesis by a SAM-dependent domain-of-unknown-function 692. . ACS Cent. Sci. 9::100818
    [Crossref] [Google Scholar]
  4. 4.
    Baesman S, Miller L, Wei J, Cho Y, Matys E, et al. 2015.. Methane oxidation and molecular characterization of methanotrophs from a former mercury mine impoundment. . Microorganisms 3::290309
    [Crossref] [Google Scholar]
  5. 5.
    Balasubramanian R, Kenney GE, Rosenzweig AC. 2011.. Dual pathways for copper uptake by methanotrophic bacteria. . J. Biol. Chem. 286::3731319
    [Crossref] [Google Scholar]
  6. 6.
    Bandow N, Gilles VS, Freesmeier B, Semrau JD, Krentz B, et al. 2012.. Spectral and copper binding properties of methanobactin from the facultative methanotroph Methylocystis strain SB2. . J. Inorg. Biochem. 110::7282
    [Crossref] [Google Scholar]
  7. 7.
    Banerjee R, Jones JC, Lipscomb JD. 2019.. Soluble methane monooxygenase. . Annu. Rev. Biochem. 88::40931
    [Crossref] [Google Scholar]
  8. 8.
    Baral BS, Bandow NL, Vorobev A, Freemeier BC, Bergman BH, et al. 2014.. Mercury binding by methanobactin from Methylocystis strain SB2. . J. Inorg. Biochem. 141::16169
    [Crossref] [Google Scholar]
  9. 9.
    Baslé A, El Ghazouani A, Lee J, Dennison C. 2018.. Insight into metal removal from peptides that sequester copper for methane oxidation. . Chem. Eur. J. 24::451518
    [Crossref] [Google Scholar]
  10. 10.
    Behling LA, Hartsel SC, Lewis DE, DiSpirito AA, Choi DW, et al. 2008.. NMR, mass spectrometry and chemical evidence reveal a different chemical structure for methanobactin that contains oxazolone rings. . J. Am. Chem. Soc. 130::126045
    [Crossref] [Google Scholar]
  11. 11.
    Braud A, Geoffroy V, Hoegy F, Mislin GLA, Schalk IJ. 2010.. Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. . Environ. Microbiol. Rep. 2::41925
    [Crossref] [Google Scholar]
  12. 12.
    Braun V, Pramanik A, Gwinner T, Köberle M, Bohn E. 2009.. Sideromycins: tools and antibiotics. . Biometals 22::313
    [Crossref] [Google Scholar]
  13. 13.
    Buettner H, Hoerl J, Krabbe J, Hertweck C. 2023.. Discovery and biosynthesis of anthrochelin, a growth-promoting metallophore of the human pathogen Luteibacter anthropi. . ChemBioChem 24::e202300322
    [Crossref] [Google Scholar]
  14. 14.
    Buglino JA, Ozakman Y, Xu Y, Chowdhury F, Tan DS, Glickman MS. 2022.. Diisonitrile lipopeptides mediate resistance to copper starvation in pathogenic mycobacteria. . mBio 13::e0251322
    [Crossref] [Google Scholar]
  15. 15.
    Burkhart BJ, Hudson GA, Dunbar KL, Mitchell DA. 2015.. A prevalent peptide-binding domain guides ribosomal natural product biosynthesis. . Nat. Chem. Biol. 11::56470
    [Crossref] [Google Scholar]
  16. 16.
    Chandrangsu P, Rensing C, Helmann JD. 2017.. Metal homeostasis and resistance in bacteria. . Nat. Rev. Microbiol. 15::33850
    [Crossref] [Google Scholar]
  17. 17.
    Chang J, Gu W, Park D, Semrau JD, Dispirito AA, Yoon S. 2018.. Methanobactin from Methylosinus trichosporium OB3b inhibits N2O reduction in denitrifiers. . ISME J. 12::208689
    [Crossref] [Google Scholar]
  18. 18.
    Chang J, Kim DD, Semrau JD, Lee JY, Heo H, et al. 2021.. Enhancement of nitrous oxide emissions in soil microbial consortia via copper competition between proteobacterial methanotrophs and denitrifiers. . Appl. Environ. Microbiol. 87::e02301
    [Crossref] [Google Scholar]
  19. 19.
    Chang J, Peng P, DiSpirito AA, Semrau JD. 2022.. Variable inhibition of nitrous oxide reduction in denitrifying bacteria by different forms of methanobactin. . Appl. Environ. Microbiol. 88::e02346
    [Crossref] [Google Scholar]
  20. 20.
    Chang J, Peng P, Farhan Ul-Haque M, Hira A, Dispirito AA, Semrau JD. 2023.. Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin. . Environ. Microbiol. 25::233850
    [Crossref] [Google Scholar]
  21. 21.
    Chioti VT, Clark CA, Ganley JG, Han EJ, Seyedsayamdost MR. 2024.. N-Cα bond cleavage catalyzed by a multinuclear iron oxygenase from a divergent methanobactin-like RiPP gene cluster. . J. Am. Chem. Soc. 146::731323
    [Crossref] [Google Scholar]
  22. 22.
    Choi D-W, Kunz RC, Boyd ES, Semrau JD, Antholine WE, et al. 2003.. The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase complex from Methylococcus capsulatus Bath. . J. Bacteriol. 185::575564
    [Crossref] [Google Scholar]
  23. 23.
    Choi DW, Bandow NL, McEllistrem MT, Semrau JD, Antholine WE, et al. 2010.. Spectral and thermodynamic properties of methanobactin from γ-proteobacterial methane oxidizing bacteria: a case for copper competition on a molecular level. . J. Inorg. Biochem. 104::124047
    [Crossref] [Google Scholar]
  24. 24.
    Choi DW, Do YS, Zea CJ, McEllistrem MT, Lee S-W, et al. 2006.. Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn(II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b. . J. Inorg. Biochem. 100::215061
    [Crossref] [Google Scholar]
  25. 25.
    Choi DW, Semrau JD, Antholine WE, Hartsel SC, Anderson RC, et al. 2008.. Oxidase, superoxide dismutase, and hydrogen peroxide reductase activities of methanobactin from types I and II methanotrophs. . J. Inorg. Biochem. 102::157180
    [Crossref] [Google Scholar]
  26. 26.
    Choi DW, Zea CJ, Do YS, Semrau JD, Antholine WE, et al. 2006.. Spectral, kinetic, and thermodynamic properties of Cu(I) and Cu(II) binding by methanobactin from Methylosinus trichosporium OB3b. . Biochemistry 45::144253
    [Crossref] [Google Scholar]
  27. 27.
    Chou JC-C, Stafford VE, Kenney GE, Dassama LMK. 2021.. The enzymology of oxazolone and thioamide synthesis in methanobactin. . Methods Enzymol. 656::34173
    [Crossref] [Google Scholar]
  28. 28.
    Cupioli E, Gaigne FJM, Sachse A, Buday P, Weigand W, et al. 2023.. Templated total synthesis of Cu(I)-methanobactin OB3b. . Angew. Chem. Int. Ed. 62::e202304901
    [Crossref] [Google Scholar]
  29. 29.
    Dassama LMK, Kenney GE, Ro SY, Zielazinski EL, Rosenzweig AC. 2016.. Methanobactin transport machinery. . PNAS 113::1302732
    [Crossref] [Google Scholar]
  30. 30.
    Dassama LMK, Kenney GE, Rosenzweig AC. 2017.. Methanobactins: from genome to function. . Metallomics 9::720
    [Crossref] [Google Scholar]
  31. 31.
    Dershwitz P, Bandow NL, Yang J, Semrau JD, McEllistrem MT, et al. 2021.. Oxygen generation via water splitting by a novel biogenic metal ion–binding compound. . Appl. Environ. Microbiol. 87::e00286
    [Crossref] [Google Scholar]
  32. 32.
    Dershwitz P, Gu W, Roche J, Kang-Yun CS, Semrau JD, et al. 2022.. MbnC is not required for the formation of the N-terminal oxazolone in the methanobactin from Methylosinus trichosporium OB3b. . Appl. Environ. Microbiol. 88::e01841
    [Crossref] [Google Scholar]
  33. 33.
    Dev S, Kruse RL, Hamilton JP, Lutsenko S. 2022.. Wilson disease: update on pathophysiology and treatment. . Front. Cell Dev. Biol. 10::871877
    [Crossref] [Google Scholar]
  34. 34.
    DiSpirito AA, Zahn JA, Graham DW, Kim HJ, Larive CK, et al. 1998.. Copper-binding compounds from Methylosinus trichosporium OB3b. . J. Bacteriol. 180::360613
    [Crossref] [Google Scholar]
  35. 35.
    Dou C, Long Z, Li S, Zhou D, Jin Y, et al. 2022.. Crystal structure and catalytic mechanism of the MbnBC holoenzyme required for methanobactin biosynthesis. . Cell Res. 32::30214
    [Crossref] [Google Scholar]
  36. 36.
    Eckert P, Johs A, Semrau JD, DiSpirito AA, Richardson J, et al. 2021.. Spectroscopic and computational investigations of organometallic complexation of group 12 transition metals by methanobactins from Methylocystis sp. SB2. . J. Inorg. Biochem. 223::111496
    [Crossref] [Google Scholar]
  37. 37.
    Einer C, Munk DE, Park E, Akdogan B, Nagel J, et al. 2023.. ARBM101 (methanobactin SB2) drains excess liver copper via biliary excretion in Wilson's disease rats. . Gastroenterology 165::187200.e7
    [Crossref] [Google Scholar]
  38. 38.
    El Ghazouani A, Baslé A, Firbank SJ, Knapp CW, Gray J, et al. 2011.. Copper-binding properties and structures of methanobactins from Methylosinus trichosporium OB3b. . Inorg. Chem. 50::137891
    [Crossref] [Google Scholar]
  39. 39.
    El Ghazouani A, Baslé A, Gray J, Graham DW, Firbank SJ, Dennison C. 2012.. Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria. . PNAS 109::84004
    [Crossref] [Google Scholar]
  40. 40.
    Ferousi C, Majer SH, DiMucci IM, Lancaster KM. 2020.. Biological and bioinspired inorganic N–N bond-forming reactions. . Chem. Rev. 120::5252307
    [Crossref] [Google Scholar]
  41. 41.
    Fitch MW, Graham DW, Arnold RG, Agarwal SK, Phelps P, et al. 1993.. Phenotypic characterization of copper-resistant mutants of Methylosinus trichosporium OB3b. . Appl. Environ. Microbiol. 59::277176
    [Crossref] [Google Scholar]
  42. 42.
    Gu W, Baral BS, DiSpirito AA, Semrau JD. 2017.. An aminotransferase is responsible for the deamination of the N-terminal leucine and required for formation of oxazolone ring A in methanobactin of Methylosinus trichosporium OB3b. . Appl. Environ. Microbiol. 83::e02619
    [Google Scholar]
  43. 43.
    Gu W, Haque MFU, Baral BS, Turpin EA, Bandow NL, et al. 2016.. A TonB-dependent transporter is responsible for methanobactin uptake by Methylosinus trichosporium OB3b. . Appl. Environ. Microbiol. 82::191723
    [Crossref] [Google Scholar]
  44. 44.
    Hakemian AS, Tinberg CE, Kondapalli KC, Telser J, Hoffman BM, et al. 2005.. The copper chelator methanobactin from Methylosinus trichosporium OB3b binds copper(I). . J. Am. Chem. Soc. 127::1714243
    [Crossref] [Google Scholar]
  45. 45.
    Hanson RS, Hanson TE. 1996.. Methanotrophic bacteria. . Microbiol. Rev. 60::43971
    [Crossref] [Google Scholar]
  46. 46.
    Helland R, Fjellbirkeland A, Karlsen OA, Ve T, Lillehaug JR, Jensen HB. 2008.. An oxidized tryptophan facilitates copper binding in Methylococcus capsulatus–secreted protein MopE. . J. Biol. Chem. 283::13897904
    [Crossref] [Google Scholar]
  47. 47.
    Hider RC, Kong X. 2010.. Chemistry and biology of siderophores. . Nat. Prod. Rep. 27::63757
    [Crossref] [Google Scholar]
  48. 48.
    Jin Z, Li J, Ni L, Zhang R, Xia A, Jin F. 2018.. Conditional privatization of a public siderophore enables Pseudomonas aeruginosa to resist cheater invasion. . Nat. Commun. 9::1383
    [Crossref] [Google Scholar]
  49. 49.
    Jodts RJ, Ho MB, Reyes RM, Park YJ, Doan PE, et al. 2024.. Initial steps in methanobactin biosynthesis: substrate binding by the mixed-valent diiron enzyme MbnBC. . Biochemistry 63::117077
    [Crossref] [Google Scholar]
  50. 50.
    Johnson KA, Ve T, Larsen Ø, Pedersen RB, Lillehaug JR, et al. 2014.. CorA is a copper repressible surface-associated copper(I)-binding protein produced in Methylomicrobium album BG8. . PLOS ONE 9::e87750
    [Crossref] [Google Scholar]
  51. 51.
    Kalidass B, Ul-Haque MF, Baral BS, DiSpirito AA, Semrau JD. 2015.. Competition between metals for binding to methanobactin enables expression of soluble methane monooxygenase in the presence of copper. . Appl. Environ. Microbiol. 81::102431
    [Crossref] [Google Scholar]
  52. 52.
    Kang-Yun CS, Liang X, Dershwitz P, Gu W, Schepers A, et al. 2022.. Evidence for methanobactin “theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation. . ISME J. 16::21120
    [Crossref] [Google Scholar]
  53. 53.
    Karlsen OA, Berven FS, Stafford GP, Larsen Ø, Murrell JC, et al. 2003.. The surface-associated and secreted MopE protein of Methylococcus capsulatus (Bath) responds to changes in the concentration of copper in the growth medium. . Appl. Environ. Microbiol. 69::238688
    [Crossref] [Google Scholar]
  54. 54.
    Kenney GE, Dassama LMK, Manesis AC, Ross MO, Chen S, et al. 2019.. MbnH is a diheme MauG-like protein associated with microbial copper homeostasis. . J. Biol. Chem. 294::1614151
    [Crossref] [Google Scholar]
  55. 55.
    Kenney GE, Dassama LMK, Pandelia M-E, Gizzi AS, Martinie RJ, et al. 2018.. The biosynthesis of methanobactin. . Science 359::141116
    [Crossref] [Google Scholar]
  56. 56.
    Kenney GE, Goering AW, Ross MO, DeHart CJ, Thomas PM, et al. 2016.. Characterization of methanobactin from Methylosinus sp. LW4. . J. Am. Chem. Soc. 138::1112427
    [Crossref] [Google Scholar]
  57. 57.
    Kenney GE, Rosenzweig AC. 2013.. Genome mining for methanobactins. . BMC Biol. 11::17
    [Crossref] [Google Scholar]
  58. 58.
    Kenney GE, Rosenzweig AC. 2018.. Chalkophores. . Annu. Rev. Biochem. 87::64576
    [Crossref] [Google Scholar]
  59. 59.
    Kenney GE, Rosenzweig AC. 2018.. Methanobactins: maintaining copper homeostasis in methanotrophs and beyond. . J. Biol. Chem. 293::460615
    [Crossref] [Google Scholar]
  60. 60.
    Kenney GE, Sadek M, Rosenzweig AC. 2016.. Copper-responsive gene expression in the methanotroph Methylosinus trichosporium OB3b. . Metallomics 8::93140
    [Crossref] [Google Scholar]
  61. 61.
    Kim HJ, Galeva N, Larive CK, Alterman M, Graham DW. 2005.. Purification and physical–chemical properties of methanobactin: a chalkophore from Methylosinus trichosporium OB3b. . Biochemistry 44::514048
    [Crossref] [Google Scholar]
  62. 62.
    Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, et al. 2004.. Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. . Science 305::161215
    [Crossref] [Google Scholar]
  63. 63.
    Koo CW, Rosenzweig AC. 2021.. Biochemistry of aerobic biological methane oxidation. . Chem. Soc. Rev. 50::342436
    [Crossref] [Google Scholar]
  64. 64.
    Koo CW, Tucci FJ, He Y, Rosenzweig AC. 2022.. Recovery of particulate methane monooxygenase structure and activity in a lipid bilayer. . Science 375::128791
    [Crossref] [Google Scholar]
  65. 65.
    Kraemer SM, Duckworth OW, Harrington JM, Schenkeveld WDC. 2015.. Metallophores and trace metal biogeochemistry. . Aquat. Geochem. 21::15995
    [Crossref] [Google Scholar]
  66. 66.
    Krentz BD, Mulheron HJ, Semrau JD, Dispirito AA, Bandow NL, et al. 2010.. A comparison of methanobactins from Methylosinus trichosporium OB3b and Methylocystis strain SB2 predicts methanobactins are synthesized from diverse peptide precursors modified to create a common core for binding and reducing copper ions. . Biochemistry 49::1011730
    [Crossref] [Google Scholar]
  67. 67.
    Kulczycki E, Fowle DA, Knapp C, Graham DW, Roberts JA. 2007.. Methanobactin-promoted dissolution of Cu-substituted borosilicate glass. . Geobiology 5::25163
    [Crossref] [Google Scholar]
  68. 68.
    Kusakizako T, Miyauchi H, Ishitani R, Nureki O. 2020.. Structural biology of the multidrug and toxic compound extrusion superfamily transporters. . Biochim. Biophys. Acta Biomembr. 1862::183154
    [Crossref] [Google Scholar]
  69. 69.
    Lee A, Winther M, Priemé A, Blunier T, Christensen S. 2017.. Hot spots of N2O emission move with the seasonally mobile oxic-anoxic interface in drained organic soils. . Soil Biol. Biochem. 115::17886
    [Crossref] [Google Scholar]
  70. 70.
    Lichtmannegger J, Leitzinger C, Wimmer R, Schmitt S, Schulz S, et al. 2016.. Methanobactin reverses acute liver failure in a rat model of Wilson disease. . J. Clin. Investig. 126::272135
    [Crossref] [Google Scholar]
  71. 71.
    Liu J, Chakraborty S, Hosseinzadeh P, Yu Y, Tian S, et al. 2014.. Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers. . Chem. Rev. 114::4366469
    [Crossref] [Google Scholar]
  72. 72.
    Lu X, Gu W, Zhao L, Farhan Ul Haque M, DiSpirito AA, et al. 2017.. Methylmercury uptake and degradation by methanotrophs. . Sci. Adv. 3::e1700041
    [Crossref] [Google Scholar]
  73. 73.
    Ma K, Conrad R, Lu Y. 2013.. Dry/wet cycles change the activity and population dynamics of methanotrophs in rice field soil. . Appl. Environ. Microbiol. 79::493239
    [Crossref] [Google Scholar]
  74. 74.
    Manesis AC, Jodts RJ, Hoffman BM, Rosenzweig AC. 2021.. Copper binding by a unique family of metalloproteins is dependent on kynurenine formation. . PNAS 118::e2100680118
    [Crossref] [Google Scholar]
  75. 75.
    Manesis AC, Slater JW, Cantave K, Martin Bollinger J, Krebs C, Rosenzweig AC. 2023.. Capturing a bis-Fe(IV) state in Methylosinus trichosporium OB3b MbnH. . Biochemistry 62::108292
    [Crossref] [Google Scholar]
  76. 76.
    Martinho M, Choi DW, Dispirito AA, Antholine WE, Semrau JD, Münck E. 2007.. Mössbauer studies of the membrane-associated methane monooxygenase from Methylococcus capsulatus Bath:evidence for a diiron center. . J. Am. Chem. Soc. 129::1578385
    [Crossref] [Google Scholar]
  77. 77.
    Montalbán-López M, Scott TA, Ramesh S, Rahman IR, Van Heel AJ, et al. 2021.. New developments in RiPP discovery, enzymology and engineering. . Nat. Prod. Rep. 38::130239
    [Crossref] [Google Scholar]
  78. 78.
    Müller J-C, Lichtmannegger J, Zischka H, Sperling M, Karst U. 2018.. High spatial resolution LA-ICP-MS demonstrates massive liver copper depletion in Wilson disease rats upon methanobactin treatment. . J. Trace Elem. Med. Biol. 49::11927
    [Crossref] [Google Scholar]
  79. 79.
    Park YJ, Jodts RJ, Slater JW, Reyes RM, Winton VJ, et al. 2022.. A mixed-valent Fe(II)Fe(III) species converts cysteine to an oxazolone/thioamide pair in methanobactin biosynthesis. . PNAS 119::e2123566119
    [Crossref] [Google Scholar]
  80. 80.
    Park YJ, Kenney GE, Schachner LF, Kelleher NL, Rosenzweig AC. 2018.. Repurposed HisC aminotransferases complete the biosynthesis of some methanobactins. . Biochemistry 57::351523
    [Crossref] [Google Scholar]
  81. 81.
    Park YJ, Roberts GM, Montaser R, Kenney GE, Thomas PM, et al. 2021.. Characterization of a copper-chelating natural product from the methanotroph Methylosinus sp. LW3. . Biochemistry 60::284550
    [Crossref] [Google Scholar]
  82. 82.
    Paul CE, Eggerichs D, Westphal AH, Tischler D, van Berkel WJH. 2021.. Flavoprotein monooxygenases: versatile biocatalysts. . Biotechnol. Adv. 51::107712
    [Crossref] [Google Scholar]
  83. 83.
    Peng P, Gu W, DiSpirito AA, Semrau JD. 2022.. Multiple mechanisms for copper uptake by Methylosinus trichosporium OB3b in the presence of heterologous methanobactin. . mBio 13::e02239
    [Google Scholar]
  84. 84.
    Peng P, Kang-Yun CS, Chang J, Gu W, DiSpirito AA, Semrau JD. 2022.. Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical “copper switch. .” Appl. Environ. Microbiol. 88::e01793
    [Google Scholar]
  85. 85.
    Perry RD, Bobrov AG, Fetherston JD. 2015.. The role of transition metal transporters for iron, zinc, manganese, and copper in the pathogenesis of Yersinia pestis. . Metallomics 7::96578
    [Crossref] [Google Scholar]
  86. 86.
    Pesch ML, Hoffmann M, Christl I, Kraemer SM, Kretzschmar R. 2013.. Competitive ligand exchange between Cu–humic acid complexes and methanobactin. . Geobiology 11::4454
    [Crossref] [Google Scholar]
  87. 87.
    Pham VN, Chang CJ. 2023.. Metalloallostery and transition metal signaling: bioinorganic copper chemistry beyond active sites. . Angew. Chem. Int. Ed. 62::e202213644
    [Crossref] [Google Scholar]
  88. 88.
    Phelps PA, Agarwal SK, Speitel GE, Georgiou G. 1992.. Methylosinus trichosporium OB3b mutants having constitutive expression of soluble methane monooxygenase in the presence of high levels of copper. . Appl. Environ. Microbiol. 58::37018
    [Crossref] [Google Scholar]
  89. 89.
    Prior SD, Dalton H. 1985.. The effect of copper ions on membrane content and methane monooxygenase activity in methanol-grown cells of Methylococcus capsulatus (Bath). . J. Gen. Microbiol. 131::15563
    [Google Scholar]
  90. 90.
    Rajakovich LJ, Zhang B, McBride MJ, Boal AK, Krebs C, Bollinger JM Jr. 2020.. 5.10 - Emerging structural and functional diversity in proteins with dioxygen-reactive dinuclear transition metal cofactors. . In Comprehensive Natural Products III, ed. H-W Liu, TP Begley , pp. 21550. Oxford, UK:: Elsevier
    [Google Scholar]
  91. 91.
    Reim A, Lüke C, Krause S, Pratscher J, Frenzel P. 2012.. One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic–anoxic interface in a flooded paddy soil. . ISME J. 6::212839
    [Crossref] [Google Scholar]
  92. 92.
    Reitz ZL, Medema MH. 2022.. Genome mining strategies for metallophore discovery. . Curr. Opin. Biotechnol. 77::102757
    [Crossref] [Google Scholar]
  93. 93.
    Ross MO, Rosenzweig AC. 2017.. A tale of two methane monooxygenases. . J. Biol. Inorg. Chem. 22::30719
    [Crossref] [Google Scholar]
  94. 94.
    Rushworth DD, Christl I, Kumar N, Hoffmann K, Kretzschmar R, et al. 2022.. Copper mobilisation from Cu sulphide minerals by methanobactin: effect of pH, oxygen and natural organic matter. . Geobiology 20::690706
    [Crossref] [Google Scholar]
  95. 95.
    Semrau JD, DiSpirito AA, Obulisamy PK, Kang-Yun CS. 2020.. Methanobactin from methanotrophs: genetics, structure, function and potential applications. . FEMS Microbiol. Lett. 367::fnaa045
    [Crossref] [Google Scholar]
  96. 96.
    Semrau JD, Jagadevan S, Dispirito AA, Khalifa A, Scanlan J, et al. 2013.. Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs. . Environ. Microbiol. 15::307786
    [Crossref] [Google Scholar]
  97. 97.
    Silale A, van den Berg B. 2023.. TonB-dependent transport across the bacterial outer membrane. . Annu. Rev. Microbiol. 77::6788
    [Crossref] [Google Scholar]
  98. 98.
    Stanley SH, Prior SD, Leak DJ, Dalton H. 1983.. Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: studies in batch and continuous cultures. . Biotechnol. Lett. 5::48792
    [Crossref] [Google Scholar]
  99. 99.
    Stein LY, Yoon S, Semrau JD, DiSpirito AA, Crombie A, et al. 2010.. Genome sequence of the obligate methanotroph Methylosinus trichosporium strain OB3b. . J. Bacteriol. 192::649798
    [Crossref] [Google Scholar]
  100. 100.
    Stenzler BR, Zhang R, Semrau JD, Dispirito AA, Poulain AJ. 2022.. Diffusion of H2S from anaerobic thiolated ligand biodegradation rapidly generates bioavailable mercury. . Environ. Microbiol. 24::321228
    [Crossref] [Google Scholar]
  101. 101.
    Stewart A, Dershwitz P, Stewart C, Sawaya MR, Yeates TO, et al. 2023.. Crystal structure of MbnF: an NADPH-dependent flavin monooxygenase from Methylocystis strain SB2. . Acta Crystallogr. F 79::11118
    [Crossref] [Google Scholar]
  102. 102.
    Summer KH, Lichtmannegger J, Bandow N, Choi DW, DiSpirito AA, Michalke B. 2011.. The biogenic methanobactin is an effective chelator for copper in a rat model for Wilson disease. . J. Trace Elem. Med. Biol. 25::3641
    [Crossref] [Google Scholar]
  103. 103.
    Téllez CM, Gaus KP, Graham DW, Arnold RG, Guzman RZ. 1998.. Isolation of copper biochelates from Methylosinus trichosporium OB3b and soluble methane monooxygenase mutants. . Appl. Environ. Microbiol. 64::111522
    [Crossref] [Google Scholar]
  104. 104.
    Tian H-J, Feng J, Zhang L-M, He J-Z, Liu Y-R. 2020.. Ecological drivers of methanotrophic communities in paddy soils around mercury mining areas. . Sci. Total Environ. 721::137760
    [Crossref] [Google Scholar]
  105. 105.
    Timofeeva AM, Galyamova MR, Sedykh SE. 2022.. Bacterial siderophores: classification, biosynthesis, perspectives of use in agriculture. . Plants 11::22
    [Google Scholar]
  106. 106.
    Tucci FJ, Jodts RJ, Hoffman BM, Rosenzweig AC. 2023.. Product analogue binding identifies the copper active site of particulate methane monooxygenase. . Nat. Catal. 6::1194204
    [Crossref] [Google Scholar]
  107. 107.
    Vangala R, Angel LA. 2021.. ESI-IM-MS reveals the metal binding of three analog methanobactin peptides with different numbers of free Cys at physiological pH. . Int. J. Mass Spectrom. 468::116640
    [Crossref] [Google Scholar]
  108. 108.
    Vorobev A, Jagadevan S, Baral BS, DiSpirito AA, Freemeier BC, et al. 2013.. Detoxification of mercury by methanobactin from Methylosinus trichosporium OB3b. . Appl. Environ. Microbiol. 79::591826
    [Crossref] [Google Scholar]
  109. 109.
    Wilson CJ, Apiyo D, Wittung-Stafshede P. 2004.. Role of cofactors in metalloprotein folding. . Q. Rev. Biophys. 37::285314
    [Crossref] [Google Scholar]
  110. 110.
    Xin J-Y, Cheng D-D, Zhang L-X, Lin K, Fan H-C, et al. 2013.. Methanobactin-mediated one-step synthesis of gold nanoparticles. . Int. J. Mol. Sci. 14::2167688
    [Crossref] [Google Scholar]
  111. 111.
    Yin X, Wang L, Zhang L, Chen H, Liang X, et al. 2020.. Synergistic effects of a chalkophore, methanobactin, on microbial methylation of mercury. . Appl. Environ. Microbiol. 86::e00122
    [Crossref] [Google Scholar]
  112. 112.
    Zhang L, Kang-Yun CS, Lu X, Chang J, Liang X, et al. 2023.. Adsorption and intracellular uptake of mercuric mercury and methylmercury by methanotrophs and methylating bacteria. . Environ. Pollut. 331::121790
    [Crossref] [Google Scholar]
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