Bacterial copper storage proteins
2018; Elsevier BV; Volume: 293; Issue: 13 Linguagem: Inglês
10.1074/jbc.tm117.000180
ISSN1083-351X
AutoresChristopher Dennison, Sholto David, Jaeick Lee,
Tópico(s)Radioactive element chemistry and processing
ResumoCopper is essential for most organisms as a cofactor for key enzymes involved in fundamental processes such as respiration and photosynthesis. However, copper also has toxic effects in cells, which is why eukaryotes and prokaryotes have evolved mechanisms for safe copper handling. A new family of bacterial proteins uses a Cys-rich four-helix bundle to safely store large quantities of Cu(I). The work leading to the discovery of these proteins, their properties and physiological functions, and how their presence potentially impacts the current views of bacterial copper handling and use are discussed in this review. Copper is essential for most organisms as a cofactor for key enzymes involved in fundamental processes such as respiration and photosynthesis. However, copper also has toxic effects in cells, which is why eukaryotes and prokaryotes have evolved mechanisms for safe copper handling. A new family of bacterial proteins uses a Cys-rich four-helix bundle to safely store large quantities of Cu(I). The work leading to the discovery of these proteins, their properties and physiological functions, and how their presence potentially impacts the current views of bacterial copper handling and use are discussed in this review. The utilization of metals by biological systems is highly paradoxical. On the one hand, metal ions provide proteins access to chemistry that would otherwise be impossible using the organic reactions that can be catalyzed by amino acid side chains. On the other hand, many of these metal ions can be toxic to cells. Copper is essential for most organisms as the cofactor for key enzymes involved in important processes such as respiration and photosynthesis (1Dennison C. Investigating the structure and function of cupredoxins.Coord. Chem. Rev. 2005; 249: 3025-305410.1016/j.ccr.2005.04.021Crossref Scopus (143) Google Scholar2Ridge P.G. Zhang Y. Gladyshev V.N. Comparative genomic analyses of copper transporters and cuproproteomes reveal evolutionary dynamics of copper utilization and its link to oxygen.PLoS ONE. 2008; 3 (18167539): e137810.1371/journal.pone.0001378Crossref PubMed Scopus (137) Google Scholar, 3Turski M.L. Thiele D.J. New roles for copper metabolism in cell proliferation, signalling and disease.J. Biol. Chem. 2009; 284 (18757361): 717-72110.1074/jbc.R800055200Abstract Full Text Full Text PDF PubMed Scopus (315) Google Scholar, 4Kim B.E. Nevitt T. Thiele D.J. Mechanisms for copper acquisition, distribution and regulation.Nat. Chem. Biol. 2008; 4 (18277979): 176-18510.1038/nchembio.72Crossref PubMed Scopus (1053) Google Scholar, 5Festa R.A. Thiele D.J. Copper: an essential metal in biology.Curr. Biol. 2011; 21 (22075424): R877-R88310.1016/j.cub.2011.09.040Abstract Full Text Full Text PDF PubMed Scopus (688) Google Scholar, 6Rensing C. McDevitt S.F. The copper metallome in prokaryotic cells.Met. Ions Life Sci. 2013; 12 (23595679): 417-45010.1007/978-94-007-5561-1_12Crossref PubMed Scopus (60) Google Scholar7Argüello J.M. Raimunda D. Padilla-Benavides T. Mechanisms of copper homeostasis in bacteria.Front. Cell Infect. Microbiol. 2013; 3 (24205499): 73Crossref PubMed Scopus (185) Google Scholar). Ideas about the cellular toxicity of copper have developed in recent years, from solely being attributed to the generation of reactive oxygen species (ROS) 2The abbreviations used are: ROSreactive oxygen speciesMTmetallothioneinCspcopper storage proteinpMMOparticulate methane monooxygenasesMMOsoluble methane monooxygenaseMbnmethanobactinTattwin-arginine translocaseBCSbathocuproine disulfonatePDBProtein Data Bank. (8Macomber L. Rensing C. Imlay J.A. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli.J. Bacteriol. 2007; 189 (17189367): 1616-162610.1128/JB.01357-06Crossref PubMed Scopus (280) Google Scholar9Macomber L. Imlay J.A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity.Proc. Natl. Acad. Sci. U.S.A. 2009; 106 (19416816): 8344-834910.1073/pnas.0812808106Crossref PubMed Scopus (803) Google Scholar, 10Chillappagari S. Seubert A. Trip H. Kuipers O.P. Marahiel M.A. Miethke M. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis.J. Bacteriol. 2010; 192 (20233928): 2512-252410.1128/JB.00058-10Crossref PubMed Scopus (170) Google Scholar11Fung D.K. Lau W.Y. Chan W.T. Yan A. Copper efflux is induced during anaerobic amino acid limitation in Escherichia coli to protect iron-sulfur cluster enzymes and biogenesis.J. Bacteriol. 2013; 195 (23893112): 4556-456810.1128/JB.00543-13Crossref PubMed Scopus (80) Google Scholar). An emerging mechanism appears to be driven by the ability of copper to bind tightly at the active sites of metalloenzymes, particularly those containing iron-sulfur clusters. This not only destroys the reactivity of the mis-metallated protein but releases iron that can produce ROS (9Macomber L. Imlay J.A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity.Proc. Natl. Acad. Sci. U.S.A. 2009; 106 (19416816): 8344-834910.1073/pnas.0812808106Crossref PubMed Scopus (803) Google Scholar). This toxicity is the reason why aquated (“free”) copper ions should not exist in cells and that copper is predicted to be highly restricted in eukaryotes (12Rae T.D. Schmidt P.J. Pufahl R.A. Culotta V.C. O'Halloran T.V. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase.Science. 1999; 284 (10221913): 805-80810.1126/science.284.5415.805Crossref PubMed Scopus (1405) Google Scholar) and prokaryotes (13Changela A. Chen K. Xue Y. Holschen J. Outten C.E. O'Halloran T.V. Mondragón A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR.Science. 2003; 301 (12958362): 1383-138710.1126/science.1085950Crossref PubMed Scopus (524) Google Scholar). Copper availability appears to be largely constrained by the use of high-affinity sites in proteins (12Rae T.D. Schmidt P.J. Pufahl R.A. Culotta V.C. O'Halloran T.V. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase.Science. 1999; 284 (10221913): 805-80810.1126/science.284.5415.805Crossref PubMed Scopus (1405) Google Scholar, 13Changela A. Chen K. Xue Y. Holschen J. Outten C.E. O'Halloran T.V. Mondragón A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR.Science. 2003; 301 (12958362): 1383-138710.1126/science.1085950Crossref PubMed Scopus (524) Google Scholar14Finney L.A. O'Halloran T.V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors.Science. 2003; 300 (12738850): 931-93610.1126/science.1085049Crossref PubMed Scopus (954) Google Scholar), although “pools” of copper bound by other molecules are important (4Kim B.E. Nevitt T. Thiele D.J. Mechanisms for copper acquisition, distribution and regulation.Nat. Chem. Biol. 2008; 4 (18277979): 176-18510.1038/nchembio.72Crossref PubMed Scopus (1053) Google Scholar, 5Festa R.A. Thiele D.J. Copper: an essential metal in biology.Curr. Biol. 2011; 21 (22075424): R877-R88310.1016/j.cub.2011.09.040Abstract Full Text Full Text PDF PubMed Scopus (688) Google Scholar, 11Fung D.K. Lau W.Y. Chan W.T. Yan A. Copper efflux is induced during anaerobic amino acid limitation in Escherichia coli to protect iron-sulfur cluster enzymes and biogenesis.J. Bacteriol. 2013; 195 (23893112): 4556-456810.1128/JB.00543-13Crossref PubMed Scopus (80) Google Scholar, 15Helbig K. Bleuel C. Krauss G.J. Nies D.H. Glutathione and transition-metal homeostasis in Escherichia coli.J. Bacteriol. 2008; 190 (18539744): 5431-543810.1128/JB.00271-08Crossref PubMed Scopus (173) Google Scholar16Outten F.W. Munson G.P. Lability and liability of endogenous copper pools.J. Bacteriol. 2013; 195 (23913325): 4553-455510.1128/JB.00891-13Crossref PubMed Scopus (9) Google Scholar, 17DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation.Microbiol. Mol. Biol. Rev. 2016; 80 (26984926): 387-40910.1128/MMBR.00058-15Crossref PubMed Scopus (92) Google Scholar18Koh E.I. Robinson A.E. Bandara N. Rogers B.E. Henderson J.P. Copper import in Escherichia coli by the yersiniabactin metallophore system.Nat. Chem. Biol. 2017; 13 (28759019): 1016-102110.1038/nchembio.2441Crossref PubMed Scopus (76) Google Scholar). reactive oxygen species metallothionein copper storage protein particulate methane monooxygenase soluble methane monooxygenase methanobactin twin-arginine translocase bathocuproine disulfonate Protein Data Bank. Approaches used by cells to enable safe copper handling, referred to as copper homeostasis, include sensors, transporters, chaperones, and insertion proteins with high affinity and specificity for copper (3Turski M.L. Thiele D.J. New roles for copper metabolism in cell proliferation, signalling and disease.J. Biol. Chem. 2009; 284 (18757361): 717-72110.1074/jbc.R800055200Abstract Full Text Full Text PDF PubMed Scopus (315) Google Scholar4Kim B.E. Nevitt T. Thiele D.J. Mechanisms for copper acquisition, distribution and regulation.Nat. Chem. Biol. 2008; 4 (18277979): 176-18510.1038/nchembio.72Crossref PubMed Scopus (1053) Google Scholar, 5Festa R.A. Thiele D.J. Copper: an essential metal in biology.Curr. Biol. 2011; 21 (22075424): R877-R88310.1016/j.cub.2011.09.040Abstract Full Text Full Text PDF PubMed Scopus (688) Google Scholar, 6Rensing C. McDevitt S.F. The copper metallome in prokaryotic cells.Met. Ions Life Sci. 2013; 12 (23595679): 417-45010.1007/978-94-007-5561-1_12Crossref PubMed Scopus (60) Google Scholar7Argüello J.M. Raimunda D. Padilla-Benavides T. Mechanisms of copper homeostasis in bacteria.Front. Cell Infect. Microbiol. 2013; 3 (24205499): 73Crossref PubMed Scopus (185) Google Scholar, 12Rae T.D. Schmidt P.J. Pufahl R.A. Culotta V.C. O'Halloran T.V. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase.Science. 1999; 284 (10221913): 805-80810.1126/science.284.5415.805Crossref PubMed Scopus (1405) Google Scholar, 13Changela A. Chen K. Xue Y. Holschen J. Outten C.E. O'Halloran T.V. Mondragón A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR.Science. 2003; 301 (12958362): 1383-138710.1126/science.1085950Crossref PubMed Scopus (524) Google Scholar14Finney L.A. O'Halloran T.V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors.Science. 2003; 300 (12738850): 931-93610.1126/science.1085049Crossref PubMed Scopus (954) Google Scholar, 19O'Halloran T.V. Culotta V.C. Metallochaperones, an intracellular shuttle service for metal ions.J. Biol. Chem. 2000; 275 (10816601): 25057-2506010.1074/jbc.R000006200Abstract Full Text Full Text PDF PubMed Scopus (679) Google Scholar20Rensing C. Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment.FEMS Microbiol. Rev. 2003; 27 (12829268): 197-21310.1016/S0168-6445(03)00049-4Crossref PubMed Scopus (568) Google Scholar, 21Solioz M. Abicht H.K. Mermod M. Mancini S. Response of Gram-positive bacteria to copper stress.J. Biol. Inorg. Chem. 2010; 15 (19774401): 3-1410.1007/s00775-009-0588-3Crossref PubMed Scopus (172) Google Scholar22Argüello J.M. Raimunda D. González-Guerrero M. Metal transport across biomembranes: emerging models for a distinct chemistry.J. Biol. Chem. 2012; 287 (22389499): 13510-1351710.1074/jbc.R111.319343Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar). A well-characterized family of copper-homeostasis proteins are the copper-transporting P-type ATPases, which can remove this metal ion from the cytosol (4Kim B.E. Nevitt T. Thiele D.J. Mechanisms for copper acquisition, distribution and regulation.Nat. Chem. Biol. 2008; 4 (18277979): 176-18510.1038/nchembio.72Crossref PubMed Scopus (1053) Google Scholar5Festa R.A. Thiele D.J. Copper: an essential metal in biology.Curr. Biol. 2011; 21 (22075424): R877-R88310.1016/j.cub.2011.09.040Abstract Full Text Full Text PDF PubMed Scopus (688) Google Scholar, 6Rensing C. McDevitt S.F. The copper metallome in prokaryotic cells.Met. Ions Life Sci. 2013; 12 (23595679): 417-45010.1007/978-94-007-5561-1_12Crossref PubMed Scopus (60) Google Scholar7Argüello J.M. Raimunda D. Padilla-Benavides T. Mechanisms of copper homeostasis in bacteria.Front. Cell Infect. Microbiol. 2013; 3 (24205499): 73Crossref PubMed Scopus (185) Google Scholar, 20Rensing C. Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment.FEMS Microbiol. Rev. 2003; 27 (12829268): 197-21310.1016/S0168-6445(03)00049-4Crossref PubMed Scopus (568) Google Scholar21Solioz M. Abicht H.K. Mermod M. Mancini S. Response of Gram-positive bacteria to copper stress.J. Biol. Inorg. Chem. 2010; 15 (19774401): 3-1410.1007/s00775-009-0588-3Crossref PubMed Scopus (172) Google Scholar, 22Argüello J.M. Raimunda D. González-Guerrero M. Metal transport across biomembranes: emerging models for a distinct chemistry.J. Biol. Chem. 2012; 287 (22389499): 13510-1351710.1074/jbc.R111.319343Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar, 23Rensing C. Fan B. Sharma R. Mitra B. Rosen B.P. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase.Proc. Natl. Acad. Sci. U.S.A. 2000; 97 (10639134): 652-65610.1073/pnas.97.2.652Crossref PubMed Scopus (417) Google Scholar24Lutsenko S. Gupta A. Burkhead J.L. Zuzel V. Cellular multitasking: the dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance.Arch. Biochem. Biophys. 2008; 476 (18534184): 22-3210.1016/j.abb.2008.05.005Crossref PubMed Scopus (172) Google Scholar). In eukaryotes, these copper-efflux pumps work with a cytosolic copper metallochaperone (ATOX1 in humans and Atx1 in yeast) to facilitate import into the trans-Golgi network for secreted copper enzymes (4Kim B.E. Nevitt T. Thiele D.J. Mechanisms for copper acquisition, distribution and regulation.Nat. Chem. Biol. 2008; 4 (18277979): 176-18510.1038/nchembio.72Crossref PubMed Scopus (1053) Google Scholar, 5Festa R.A. Thiele D.J. Copper: an essential metal in biology.Curr. Biol. 2011; 21 (22075424): R877-R88310.1016/j.cub.2011.09.040Abstract Full Text Full Text PDF PubMed Scopus (688) Google Scholar, 19O'Halloran T.V. Culotta V.C. Metallochaperones, an intracellular shuttle service for metal ions.J. Biol. Chem. 2000; 275 (10816601): 25057-2506010.1074/jbc.R000006200Abstract Full Text Full Text PDF PubMed Scopus (679) Google Scholar, 24Lutsenko S. Gupta A. Burkhead J.L. Zuzel V. Cellular multitasking: the dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance.Arch. Biochem. Biophys. 2008; 476 (18534184): 22-3210.1016/j.abb.2008.05.005Crossref PubMed Scopus (172) Google Scholar, 25Pufahl R.A. Singer C.P. Peariso K.L. Lin S.J. Schmidt P.J. Fahrni C.J. Culotta V.C. Penner-Hahn J.E. O'Halloran T.V. Metal ion chaperone function of the soluble Cu(I) receptor Atx1.Science. 1997; 278 (9346482): 853-85610.1126/science.278.5339.853Crossref PubMed Scopus (603) Google Scholar). The two Cu-ATPases in humans (ATP7A and ATP7B) can relocate to the plasma membrane to remove excess intracellular copper when necessary (4Kim B.E. Nevitt T. Thiele D.J. Mechanisms for copper acquisition, distribution and regulation.Nat. Chem. Biol. 2008; 4 (18277979): 176-18510.1038/nchembio.72Crossref PubMed Scopus (1053) Google Scholar, 24Lutsenko S. Gupta A. Burkhead J.L. Zuzel V. Cellular multitasking: the dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance.Arch. Biochem. Biophys. 2008; 476 (18534184): 22-3210.1016/j.abb.2008.05.005Crossref PubMed Scopus (172) Google Scholar). In bacteria, the production of the copper-efflux pump CopA (23Rensing C. Fan B. Sharma R. Mitra B. Rosen B.P. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase.Proc. Natl. Acad. Sci. U.S.A. 2000; 97 (10639134): 652-65610.1073/pnas.97.2.652Crossref PubMed Scopus (417) Google Scholar) is controlled by transcriptional regulators (sensors) such as CueR (13Changela A. Chen K. Xue Y. Holschen J. Outten C.E. O'Halloran T.V. Mondragón A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR.Science. 2003; 301 (12958362): 1383-138710.1126/science.1085950Crossref PubMed Scopus (524) Google Scholar) and CsoR (26Liu T. Ramesh A. Ma Z. Ward S.K. Zhang L. George G.N. Talaat A.M. Sacchettini J.C. Giedroc D.P. CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator.Nat. Chem. Biol. 2007; 3 (17143269): 60-6810.1038/nchembio844Crossref PubMed Scopus (261) Google Scholar). CopA can work either alone or in concert with the ATOX1/Atx1 homologue CopZ to remove cytosolic copper (5Festa R.A. Thiele D.J. Copper: an essential metal in biology.Curr. Biol. 2011; 21 (22075424): R877-R88310.1016/j.cub.2011.09.040Abstract Full Text Full Text PDF PubMed Scopus (688) Google Scholar, 6Rensing C. McDevitt S.F. The copper metallome in prokaryotic cells.Met. Ions Life Sci. 2013; 12 (23595679): 417-45010.1007/978-94-007-5561-1_12Crossref PubMed Scopus (60) Google Scholar7Argüello J.M. Raimunda D. Padilla-Benavides T. Mechanisms of copper homeostasis in bacteria.Front. Cell Infect. Microbiol. 2013; 3 (24205499): 73Crossref PubMed Scopus (185) Google Scholar, 20Rensing C. Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment.FEMS Microbiol. Rev. 2003; 27 (12829268): 197-21310.1016/S0168-6445(03)00049-4Crossref PubMed Scopus (568) Google Scholar21Solioz M. Abicht H.K. Mermod M. Mancini S. Response of Gram-positive bacteria to copper stress.J. Biol. Inorg. Chem. 2010; 15 (19774401): 3-1410.1007/s00775-009-0588-3Crossref PubMed Scopus (172) Google Scholar, 22Argüello J.M. Raimunda D. González-Guerrero M. Metal transport across biomembranes: emerging models for a distinct chemistry.J. Biol. Chem. 2012; 287 (22389499): 13510-1351710.1074/jbc.R111.319343Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar23Rensing C. Fan B. Sharma R. Mitra B. Rosen B.P. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase.Proc. Natl. Acad. Sci. U.S.A. 2000; 97 (10639134): 652-65610.1073/pnas.97.2.652Crossref PubMed Scopus (417) Google Scholar, 27Cobine P. Wickramasinghe W.A. Harrison M.D. Weber T. Solioz M. Dameron C.T. The Enterococcus hirae copper chaperone CopZ delivers copper(I) to the CopY repressor.FEBS Lett. 1999; 445 (10069368): 27-3010.1016/S0014-5793(99)00091-5Crossref PubMed Scopus (139) Google Scholar, 28Banci L. Bertini I. Del Conte R. Markey J. Ruiz-Dueñas F.J. Copper trafficking: the solution structure of Bacillus subtilis CopZ.Biochemistry. 2001; 40 (11747441): 15660-1566810.1021/bi0112715Crossref PubMed Scopus (103) Google Scholar). It has recently been found that in bacteria not previously thought to possess this copper metallochaperone, such as Escherichia coli, CopZ can be made from the CopA gene by “programmed ribosomal frameshifting” (29Meydan S. Klepacki D. Karthikeyan S. Margus T. Thomas P. Jones J.E. Khan Y. Briggs J. Dinman J.D. Vázquez-Laslop N. Mankin A.S. Programmed ribosomal frameshifting generates a copper transporter and a copper chaperone from the same gene.Mol. Cell. 2017; 65 (28107647): 207-21910.1016/j.molcel.2016.12.008Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar). It is emerging that the human immune system uses the toxicity of copper to attack invading pathogens. Previous minireviews in the “Thematic Series on Metals in Biology” have discussed copper biochemistry (3Turski M.L. Thiele D.J. New roles for copper metabolism in cell proliferation, signalling and disease.J. Biol. Chem. 2009; 284 (18757361): 717-72110.1074/jbc.R800055200Abstract Full Text Full Text PDF PubMed Scopus (315) Google Scholar, 22Argüello J.M. Raimunda D. González-Guerrero M. Metal transport across biomembranes: emerging models for a distinct chemistry.J. Biol. Chem. 2012; 287 (22389499): 13510-1351710.1074/jbc.R111.319343Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar), emphasizing its role in pathogenicity (30Hodgkinson V. Petris M.J. Copper homeostasis at the host-pathogen interface.J. Biol. Chem. 2012; 287 (22389498): 13549-1355510.1074/jbc.R111.316406Abstract Full Text Full Text PDF PubMed Scopus (223) Google Scholar31García-Santamarina S. Thiele D.J. Copper at the fungal pathogen-host axis.J. Biol. Chem. 2015; 290 (26055724): 18945-1895310.1074/jbc.R115.649129Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 32Djoko K.Y. Ong C.I. Walker M.J. McEwan A.G. The role of copper and zinc toxicity in innate immune defense against bacterial pathogens.J. Biol. Chem. 2015; 290 (26055706): 18954-1896110.1074/jbc.R115.647099Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar, 33Darwin K.H. Mycobacterium tuberculosis and copper: a newly appreciated defense against an old foe?.J. Biol. Chem. 2015; 290 (26055711): 18962-1896610.1074/jbc.R115.640193Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar34Koh E.I. Henderson J.P. Microbial copper-binding siderophores at the host-pathogen interface.J. Biol. Chem. 2015; 290 (26055720): 18967-1897410.1074/jbc.R115.644328Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar). We will therefore only touch on this issue briefly toward the end of our minireview. The main topic here is the recently discovered ability of bacteria to safely store copper using a highly novel approach (35Vita N. Platsaki S. Baslé A. Allen S.J. Paterson N.G. Crombie A.T. Murrell J.C. Waldron K.J. Dennison C. A four-helix bundle stores copper for methane oxidation.Nature. 2015; 525 (26308900): 140-14310.1038/nature14854Crossref PubMed Scopus (62) Google Scholar). The more widespread and abundant class of the new family of bacterial proteins that can perform this function is cytosolic (36Vita N. Landolfi G. Baslé A. Platsaki S. Lee J. Waldron K.J. Dennison C. Bacterial cytosolic proteins with a high capacity for Cu(I) that protects against copper toxicity.Sci. Rep. 2016; 6 (27991525): 3906510.1038/srep39065Crossref PubMed Scopus (38) Google Scholar). This is somewhat controversial, as a widely accepted view is that bacteria have evolved not to use cytosolic copper enzymes as a way to help avoid the potential toxicity associated with their metalation (6Rensing C. McDevitt S.F. The copper metallome in prokaryotic cells.Met. Ions Life Sci. 2013; 12 (23595679): 417-45010.1007/978-94-007-5561-1_12Crossref PubMed Scopus (60) Google Scholar, 13Changela A. Chen K. Xue Y. Holschen J. Outten C.E. O'Halloran T.V. Mondragón A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR.Science. 2003; 301 (12958362): 1383-138710.1126/science.1085950Crossref PubMed Scopus (524) Google Scholar, 37Tottey S. Waldron K.J. Firbank S.J. Reale B. Bessant C. Sato K. Cheek T.R. Gray J. Banfield M.J. Dennison C. Robinson N.J. Protein-folding location can regulate manganese-binding versus copper- or zinc-binding.Nature. 2008; 455 (18948958): 1138-114210.1038/nature07340Crossref PubMed Scopus (252) Google Scholar). Eukaryotes are able to store cytosolic copper using metallothioneins (MTs) (38Pountney D.L. Schauwecker I. Zarn J. Vasák M. Formation of mammalian Cu8-metallothionein in vitro: evidence for the existence of two Cu(I)4-thiolate clusters.Biochemistry. 1994; 33 (8068648): 9699-970510.1021/bi00198a040Crossref PubMed Scopus (99) Google Scholar39Calderone V. Dolderer B. Hartmann H.J. Echner H. Luchinat C. Del Bianco C. Mangani S. Weser U. The crystal structure of yeast copper thionein: the solution of a long-lasting enigma.Proc. Natl. Acad. Sci. U.S.A. 2005; 102 (15613489): 51-5610.1073/pnas.0408254101Crossref PubMed Scopus (127) Google Scholar, 40Banci L. Bertini I. Ciofi-Baffoni S. Kozyreva T. Zovo K. Palumaa P. Affinity gradients drive copper to cellular destinations.Nature. 2010; 465 (20463663): 645-64810.1038/nature09018Crossref PubMed Scopus (369) Google Scholar41Sutherland D.E. Stillman M.J. The “magic numbers” of metallothionein.Metallomics. 2011; 3 (21409206): 444-46310.1039/c0mt00102cCrossref PubMed Scopus (165) Google Scholar). Related proteins have been characterized in pathogenic mycobacteria (42Gold B. Deng H. Bryk R. Vargas D. Eliezer D. Roberts J. Jiang X. Nathan C. Identification of a copper-binding metallothionein in pathogenic mycobacteria.Nat. Chem. Biol. 2008; 4 (18724363): 609-61610.1038/nchembio.109Crossref PubMed Scopus (166) Google Scholar), but the idea that bacterial copper storage systems could be more common was unknown. This changed with the discovery of a new family of copper storage proteins, the Csps, in the methane-oxidizing bacterium (methanotroph) Methylosinus trichosporium OB3b (35Vita N. Platsaki S. Baslé A. Allen S.J. Paterson N.G. Crombie A.T. Murrell J.C. Waldron K.J. Dennison C. A four-helix bundle stores copper for methane oxidation.Nature. 2015; 525 (26308900): 140-14310.1038/nature14854Crossref PubMed Scopus (62) Google Scholar). It is not surprising that such a finding about copper biochemistry was made in methanotrophs as these Gram-negative organisms use large amounts of copper to metabolize methane via the membrane-bound (particulate) methane monooxygenase (pMMO). This enzyme catalyzes the conversion of methane to methanol in almost all methanotrophs (17DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation.Microbiol. Mol. Biol. Rev. 2016; 80 (26984926): 387-40910.1128/MMBR.00058-15Crossref PubMed Scopus (92) Google Scholar). pMMO, originally thought to have a dinuclear copper-active site, but which has very recently been suggested to be mononuclear (43Cao L. Caldararu O. Rosenzweig A.C. Ryde U. Quantum refinement does not support dinuclear copper sites in crystal structure of particulate methane monooxygenase.Angew. Chem. Int. Ed. Engl. 2018; 57 (29164769): 162-16610.1002/anie.201708977Crossref PubMed Scopus (106) Google Scholar), is housed on specialized intracytoplasmic membranes (17DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation.Microbiol. Mol. Biol. Rev. 2016; 80 (26984926): 387-40910.1128/MMBR.00058-15Crossref PubMed Scopus (92) Google Scholar, 44Hanson R.S. Hanson T.E. Methanotrophic bacteria.Microbiol. Rev. 1996; 60 (8801441): 439-471Crossref PubMed Google Scholar) and can constitute a large proportion of total cellular protein. When copper levels are low, some methanotrophs (17DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation.Microbiol. Mol. Biol. Rev. 2016; 80 (26984926): 387-40910.1128/MMBR.00058-15Crossref PubMed Scopus (92) Google Scholar, 45Murrell J.C. McDonald I.R. Gilbert B. Regulation of expression of methane monooxygenases by copper ions.Trends Microbiol. 2000; 8 (10785638): 221-22510.1016/S0966-842X(00)01739-XAbstract Full Text Full Text PDF PubMed Scopus (194) Google Scholar) have the ability to use the soluble MMO (sMMO), which has a dinuclear iron-active site (46Rosenzweig A.C. Frederick C.A. Lippard S.J. Nordlund P. Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane.Nature. 1993; 366 (8255292): 537-54310.1038/366537a0Crossref PubMed Scopus (866) Google Scholar). The switchover between these MMOs is copper-regulated, and more detail about this process and methanotroph classification and metabolism can be found in Ref. 17DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation.Microbiol. Mol. Biol. Rev. 2016; 80 (26984926): 387-40910.1128/MMBR.00058-15Crossref PubMed Scopus (92) Google Scholar. Understanding how methanotrophs manage and use copper has immense environmental relevance due to methane being a highly potent greenhouse gas, and it is also essential for prospective biotechnological applications of these organisms and their MMOs (47Jiang H. Chin Y. Jiang P. Zhang C. Smith T.J. Murrell J.C. Xing X. Methanotrophs: multifunctional bacteria with promising applications in environmental bioengineering.Biochem. Eng. J. 2010; 49: 277-28810.1016/j.bej.2010.01.003Crossref Scopus (154) Google Scholar, 48Haynes C.A. Gonzalez R. Rethinking biological activation of methane and conversion to liquid fuels.Nat. Chem. Biol. 2014; 10 (24743257): 331-33910.1038/nchembio.1509Crossref PubMed Scopus (227) Google Scholar49Kalyuzhnaya M.G. Puri A.W. Lidstrom M.E. Metabolic engineering in methanotrophic bacteria.Metab. Eng. 2015; 29 (25825038): 142-15210.1016/j.ymben.2015.03.010Crossref PubMed Scopus (244) Google Scholar). The ability to utilize large amounts of copper results in methanotrophs having highly interesting copper-handling systems. This includes methanobactin (Mbn) (17DiSpirito A.A. Semrau J.D. Murrell J.C. Gallagher W.H. Dennison C. Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation.Microbiol. Mol. Biol. Rev. 2016; 80 (26984926): 387-40910.1128/MMBR.00058-15Crossref PubMed Scopus (92) Google Scholar, 50Kim H.J. Graham D.W. Dispirito A.A. Alterman M.A. Galeva N. Larive C.K. Asunskis D. Sherwood P.M. Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria.Science. 2004; 305 (15361623): 1612-161510.1126/science.1098322Crossref PubMed Scopus (265) Google Scholar, 51Krentz B.D. Mulheron H.J. Semrau J.D. Dispirito A.A. Bandow N.L. Haft D.H. Vuilleumier S. Murrell J.C. McEllistrem M.T. Hartsel S.C. Gallagher W.H. 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 c
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