Metal homeostasis and resistance in bacteria
Open accessAbstract
Metal ions are essential for many reactions, but excess metals can be toxic. In bacteria, metal limitation activates pathways that are involved in the import and mobilization of metals, whereas excess metals induce efflux and storage. In this Review, we highlight recent insights into metal homeostasis, including protein-based and RNA-based sensors that interact directly with metals or metal-containing cofactors. The resulting transcriptional response to metal stress takes place in a stepwise manner and is reinforced by post-transcriptional regulatory systems. Metal limitation and intoxication by the host are evolutionarily ancient strategies for limiting bacterial growth. The details of the resulting growth restriction are beginning to be understood and seem to be organism-specific.
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Fe2+ is the dominant oxidation state in the labile iron pool.
“The transition metals Mn2+ and Fe2+ (the dominant oxidation state in the labile pool) have a moderate affinity for ligands and cells have lower quotas (often ∼0.1 to 1 mM).1,10,11”
From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [1]
The Metalloregulatory systems section describes a labile iron pool and estimates a free Fe(II) pool in B. subtilis. It does not say that Fe(II) is the dominant oxidation state in the labile iron pool or compare its abundance with other iron oxidation states. Page numbers are unavailable in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe transition metals Mn2+ and Fe2+ have a moderate affinity for ligands.
“The transition metals Mn2+ and Fe2+ (the dominant oxidation state in the labile pool) have a moderate affinity for ligands and cells have lower quotas (often ∼0.1 to 1 mM).1,10,11”
From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [1]
Labile cation pools are sensed by metalloregulatory systems and serve to metalate nascent metalloproteins.
“The labile cation pools are sensed by metalloregulatory systems1,219 and serve to metalate nascent metalloproteins.3”
From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [1]
For regulators of metal import, the set-point defines the boundary between metal deficiency and sufficiency, whereas for regulators of efflux and storage, the set-point delineates the boundary between sufficiency and excess.
“For regulators of metal import, the set-point defines the boundary between metal deficiency and sufficiency, whereas for regulators of efflux and storage, the set-point delineates the boundary between sufficiency and excess.1”
From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [1]
Cells have lower quotas for Mn and Fe, often ∼0.1 to 1 mM.
“The transition metals Mn2+ and Fe2+ (the dominant oxidation state in the labile pool) have a moderate affinity for ligands and cells have lower quotas (often ∼0.1 to 1 mM).1,10,11”
From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [1]
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Cites
Cloning and characterization of a mammalian proton-coupled metal-ion transporter
Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L., & Hediger, M. A. (1997) · Nature · doi:10.1038/41343 · Cited by 3,166 · see citing works
Andrews, S. C., Robinson, A. K., & Rodríguez-Quiñones, F. (2003) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(03)00055-x · Cited by 2,702 · see citing works
Nutritional immunity: transition metals at the pathogen–host interface
Hood, M. I., & Skaar, E. P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2836 · Cited by 1,535 · see citing works
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis
Outten, C. E., & O'Halloran, A. T. V. (2001) · Science · doi:10.1126/science.1060331 · Cited by 1,489 · see citing works
The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation
Lee, J.-W., & Helmann, J. D. (2006) · Nature · doi:10.1038/nature04537 · Cited by 547 · see citing works
Self-citationLack of a role for iron in the Lyme disease pathogen
Posey, J. E., & Gherardini, F. C. (2000) · Science · doi:10.1126/science.288.5471.1651 · Cited by 538 · see citing works
A Role for the ATP7A Copper-transporting ATPase in Macrophage Bactericidal Activity
White, C., Lee, J., Kambe, T., Fritsche, K., & Petris, M. J. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.070201 · Cited by 524 · see citing works
The ZnuABC high‐affinity zinc uptake system and its regulator Zur in <i>Escherichia coli</i>
Patzer, S. I., & Hantke, K. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00883.x · Cited by 490 · see citing works
A Molecular Mechanism for Bacterial Susceptibility to Zinc
McDevitt, C. A., Ogunniyi, A. D., Valkov, E., Lawrence, M. C., Kobe, B., McEwan, A. G., & Paton, J. C. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002357 · Cited by 484 · see citing works
Functional specialization within the Fur family of metalloregulators
Lee, J.-W., & Helmann, J. D. (2007) · BioMetals · doi:10.1007/s10534-006-9070-7 · Cited by 432 · see citing works
Self-citationStructure and Mechanism of a Metal-Sensing Regulatory RNA
Dann, C. E., Wakeman, C. A., Sieling, C. L., Baker, S. C., Irnov, I., & Winkler, W. C. (2007) · Cell · doi:10.1016/j.cell.2007.06.051 · Cited by 386 · see citing works
Mycobacterial P1-Type ATPases Mediate Resistance to Zinc Poisoning in Human Macrophages
Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., Wang, C., Tailleux, L., Tilleul, S., Charrière, G. M., et al. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.08.006 · Cited by 381 · see citing works
Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., Restrepo, N. A., Hosking, M. P., Edwards, R. A., Battistoni, A., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.01.017 · Cited by 328 · see citing works
Pohl, E., Haller, J. C., Mijovilovich, A., Meyer‐Klaucke, W., Garman, E., & Vasil, M. L. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03337.x · Cited by 326 · see citing works
Que, Q., & Helmann, J. D. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01811.x · Cited by 282 · see citing works
Self-citationGlobal analysis of the <i>Bacillus subtilis</i> Fur regulon and the iron starvation stimulon
Baichoo, N., Wang, T., Ye, R., & Helmann, J. D. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03113.x · Cited by 250 · see citing works
Self-citationBacterial Strategies to Maintain Zinc Metallostasis at the Host-Pathogen Interface
Capdevila, D. A., Wang, J., & Giedroc, D. P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.742023 · Cited by 181 · see citing works
Sheikh, M. A., & Taylor, G. L. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06718.x · Cited by 126 · see citing works
Deng, Z., Wang, Q., Liu, Z., Zhang, M., Machado, A. C. D., Chiu, T.-P., Feng, C., Zhang, Q., Yu, L., Qi, L., et al. (2015) · Nature Communications · doi:10.1038/ncomms8642 · Cited by 117 · see citing works
Zinc disrupts central carbon metabolism and capsule biosynthesis in Streptococcus pyogenes
Ong, C.-L. Y., Walker, M. J., & McEwan, A. G. (2015) · Scientific Reports · doi:10.1038/srep10799 · Cited by 107 · see citing works
Fung, D. K. C., Lau, W. Y., Chan, W. T., & Yan, A. (2013) · Journal of Bacteriology · doi:10.1128/jb.00543-13 · Cited by 99 · see citing works
Turner, A. G., Ong, C.-L. Y., Gillen, C. M., Davies, M. R., West, N. P., McEwan, A. G., & Walker, M. J. (2015) · mBio · doi:10.1128/mbio.00278-15 · Cited by 93 · see citing works
Trace Element Requirements of Lactobacillus acidophilus
SABINE, D. B., & VASELEKOS, J. (1967) · Nature · doi:10.1038/214520a0 · Cited by 22 · see citing works
Flagged first, then by citations
Research works printed but not linked: 151
- [1]Merchant SS Helmann JD Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation Advances in microbial physiology 60 91 210 10.1016/b978-0-12-398264-3.00002-4 2012 22633059 PMC4100946 · DOI · Paper page
- [3]Djoko KY Ong CL Walker MJ McEwan AG The Role of Copper and Zinc Toxicity in Innate Immune Defense against Bacterial Pathogens The Journal of biological chemistry 290 18954 18961 10.1074/jbc.R115.647099 2015 26055706 PMC4521016 · DOI · Paper page
- [4]Ma Z Jacobsen FE Giedroc DP Coordination chemistry of bacterial metal transport and sensing Chemical reviews 109 4644 4681 10.1021/cr900077w 2009 19788177 PMC2783614 · DOI
- [5]Waldron KJ Rutherford JC Ford D Robinson NJ Metalloproteins and metal sensing Nature 460 823 830 10.1038/nature08300 2009 19675642 · DOI · Paper page
- [6]Mettert EL Kiley PJ Fe-S proteins that regulate gene expression Biochimica et biophysica acta 1853 1284 1293 10.1016/j.bbamcr.2014.11.018 2015 25450978 PMC4390428 · DOI
- [7]O’Brian MR Perception and Homeostatic Control of Iron in the Rhizobia and Related Bacteria Annual review of microbiology 69 229 245 10.1146/annurev-micro-091014-104432 2015 26195304 · DOI
- [8]Cromie MJ Shi Y Latifi T Groisman EA An RNA sensor for intracellular Mg(2+) Cell 125 71 84 10.1016/j.cell.2006.01.043 2006 16615891 · DOI
- [9]Price IR Gaballa A Ding F Helmann JD Ke A Mn(2+)-sensing mechanisms of yybP-ykoY orphan riboswitches Molecular cell 57 1110 1123 10.1016/j.molcel.2015.02.016 2015 25794619 PMC4703321 · DOI · Paper page
- [10]Dambach M The ubiquitous yybP-ykoY riboswitch is a manganese-responsive regulatory element Molecular cell 57 1099 1109 10.1016/j.molcel.2015.01.035 2015 25794618 PMC4376352 · DOI
- [11]Nies DH Efflux-mediated heavy metal resistance in prokaryotes FEMS microbiology reviews 27 313 339 2003 12829273
- [12]Colvin RA Holmes WR Fontaine CP Maret W Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis Metallomics: integrated biometal science 2 306 317 10.1039/b926662c 2010 21069178 · DOI
- [14]Sankaran B Zinc-independent folate biosynthesis: genetic, biochemical, and structural investigations reveal new metal dependence for GTP cyclohydrolase IB Journal of bacteriology 191 6936 6949 10.1128/jb.00287-09 2009 19767425 PMC2772490 · DOI
- [15]Natori Y A fail-safe system for the ribosome under zinc-limiting conditions in Bacillus subtilis Molecular microbiology 63 294 307 10.1111/j.1365-2958.2006.05513.x 2007 17163968 · DOI
- [16]Martin JE Imlay JA The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation Molecular microbiology 80 319 334 10.1111/j.1365-2958.2011.07593.x 2011 21338418 PMC3097424 · DOI
- [17]Imlay JA The mismetallation of enzymes during oxidative stress The Journal of biological chemistry 289 28121 28128 10.1074/jbc.R114.588814 2014 25160623 PMC4192467 · DOI
- [18]Huang X Shin JH Pinochet-Barros A Su TT Helmann JD Bacillus subtilis MntR coordinates the transcriptional regulation of manganese uptake and efflux systems Molecular microbiology 10.1111/mmi.13554 2016 PMC5218975 27748968 · DOI · Paper page
- [19]Waters LS Sandoval M Storz G The Escherichia coli MntR miniregulon includes genes encoding a small protein and an efflux pump required for manganese homeostasis Journal of bacteriology 193 5887 5897 10.1128/jb.05872-11 2011 21908668 PMC3194919 · DOI
- [20]Rosch JW Gao G Ridout G Wang YD Tuomanen EI Role of the manganese efflux system mntE for signalling and pathogenesis in Streptococcus pneumoniae Molecular microbiology 72 12 25 10.1111/j.1365-2958.2009.06638.x 2009 19226324 PMC2706702 · DOI · Paper page
- [21]Hantke K Bacterial zinc transporters and regulators Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine 14 239 249 2001 11831459
- [22]Rensing C Grass G Escherichia coli mechanisms of copper homeostasis in a changing environment FEMS microbiology reviews 27 197 213 2003 12829268
- [23]Guan G PfeT, a P1B4 -type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication Molecular microbiology 98 787 803 10.1111/mmi.13158 2015 26261021 PMC4648274 · DOI · Paper page
- [24]Pi H Patel SJ Arguello JM Helmann JD The Listeria monocytogenes Fur-regulated virulence protein FrvA is an Fe(II) efflux P1B4 -type ATPase Molecular microbiology 100 1066 1079 10.1111/mmi.13368 2016 26946370 PMC4914386 · DOI
- [26]Patel SJ Fine-tuning of Substrate Affinity Leads to Alternative Roles of Mycobacterium tuberculosis Fe2+-ATPases The Journal of biological chemistry 291 11529 11539 10.1074/jbc.M116.718239 2016 27022029 PMC4882424 · DOI
- [27]Weinberg ED Nutritional immunity. Host’s attempt to withold iron from microbial invaders Jama 231 39 41 1975 1243565
- [28]Skaar EP Raffatellu M Metals in infectious diseases and nutritional immunity Metallomics: integrated biometal science 7 926 928 10.1039/c5mt90021b 2015 26017093 · DOI · Paper page
- [31]Anjem A Varghese S Imlay JA Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli Molecular microbiology 72 844 858 10.1111/j.1365-2958.2009.06699.x 2009 19400769 PMC2776087 · DOI · Paper page
- [32]Vasantha N Freese E The role of manganese in growth and sporulation of Bacillus subtilis Journal of general microbiology 112 329 336 10.1099/00221287-112-2-329 1979 225409 · DOI
- [33]Waldron KJ Robinson NJ How do bacterial cells ensure that metalloproteins get the correct metal? Nature reviews. Microbiology 7 25 35 10.1038/nrmicro2057 2009 19079350 · DOI
- [34]Gaballa A Helmann JD Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis Journal of bacteriology 180 5815 5821 1998 9811636 PMC107652
- [35]Moore CM Helmann JD Metal ion homeostasis in Bacillus subtilis Current opinion in microbiology 8 188 195 10.1016/j.mib.2005.02.007 2005 15802251 · DOI
- [36]Bsat N Herbig A Casillas-Martinez L Setlow P Helmann JD Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors Molecular microbiology 29 189 198 1998 9701813
- [38]Hantke K Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12 Molecular & general genetics: MGG 197 337 341 1984 6097798
- [40]Dian C The structure of the Helicobacter pylori ferric uptake regulator Fur reveals three functional metal binding sites Molecular microbiology 79 1260 1275 10.1111/j.1365-2958.2010.07517.x 2011 21208302 · DOI
- [41]Butcher J Sarvan S Brunzelle JS Couture JF Stintzi A Structure and regulon of Campylobacter jejuni ferric uptake regulator Fur define apo-Fur regulation Proceedings of the National Academy of Sciences of the United States of America 109 10047 10052 10.1073/pnas.1118321109 2012 22665794 PMC3382491 · DOI · Paper page
- [44]Gaballa A MacLellan S Helmann JD Transcription activation by the siderophore sensor Btr is mediated by ligand-dependent stimulation of promoter clearance Nucleic acids research 40 3585 3595 10.1093/nar/gkr1280 2012 22210890 PMC3333878 · DOI
- [46]Funahashi T Characterization of Vibrio parahaemolyticus manganese-resistant mutants in reference to the function of the ferric uptake regulatory protein Microbiology and immunology 44 963 970 2000 11220684
- [47]Benson HP LeVier K Guerinot ML A dominant-negative fur mutation in Bradyrhizobium japonicum Journal of bacteriology 186 1409 1414 2004 14973020 PMC344408
- [48]Hantke K Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism Molecular & general genetics: MGG 210 135 139 1987 3323834
- [49]Merchant AT Spatafora GA A role for the DtxR family of metalloregulators in gram-positive pathogenesis Molecular oral microbiology 29 1 10 10.1111/omi.12039 2014 24034418 PMC3866218 · DOI
- [50]Kliegman JI Griner SL Helmann JD Brennan RG Glasfeld A Structural basis for the metal-selective activation of the manganese transport regulator of Bacillus subtilis Biochemistry 45 3493 3505 10.1021/bi0524215 2006 16533030 PMC2586665 · DOI
- [51]McGuire AM Roles of the A and C sites in the manganese-specific activation of MntR Biochemistry 52 701 713 10.1021/bi301550t 2013 23298157 PMC3562352 · DOI
- [52]Patzer SI Hantke K Dual repression by Fe(2+)-Fur and Mn(2+)-MntR of the mntH gene, encoding an NRAMP-like Mn(2+) transporter in Escherichia coli Journal of bacteriology 183 4806 4813 10.1128/jb.183.16.4806-4813.2001 2001 11466284 PMC99535 · DOI
- [53]Ikeda JS Janakiraman A Kehres DG Maguire ME Slauch JM Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur Journal of bacteriology 187 912 922 10.1128/jb.187.3.912-922.2005 2005 15659669 PMC545731 · DOI
- [55]Ma Z Lee JW Helmann JD Identification of altered function alleles that affect Bacillus subtilis PerR metal ion selectivity Nucleic acids research 39 5036 5044 10.1093/nar/gkr095 2011 21398634 PMC3130269 · DOI
- [56]Moore CM Gaballa A Hui M Ye RW Helmann JD Genetic and physiological responses of Bacillus subtilis to metal ion stress Molecular microbiology 57 27 40 10.1111/j.1365-2958.2005.04642.x 2005 15948947 · DOI
- [57]Pennella MA Arunkumar AI Giedroc DP Individual metal ligands play distinct functional roles in the zinc sensor Staphylococcus aureus CzrA Journal of molecular biology 356 1124 1136 10.1016/j.jmb.2005.12.019 2006 16406068 · DOI
- [59]Hamza I Qi Z King ND O’Brian MR Fur-independent regulation of iron metabolism by Irr in Bradyrhizobium japonicum Microbiology (Reading, England) 146 Pt 3 669 676 10.1099/00221287-146-3-669 2000 10746770 · DOI
- [60]Qi Z O’Brian MR Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis Molecular cell 9 155 162 2002 11804594
- [61]Rudolph G The Iron control element, acting in positive and negative control of iron-regulated Bradyrhizobium japonicum genes, is a target for the Irr protein Journal of bacteriology 188 733 744 10.1128/jb.188.2.733-744.2006 2006 16385063 PMC1347296 · DOI
- [62]Ferreira GC Heme biosynthesis: biochemistry, molecular biology, and relationship to disease Journal of bioenergetics and biomembranes 27 147 150 1995 7592561
- [63]Schwartz CJ IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins Proceedings of the National Academy of Sciences of the United States of America 98 14895 14900 10.1073/pnas.251550898 2001 11742080 PMC64955 · DOI
- [64]Giel JL Rodionov D Liu M Blattner FR Kiley PJ IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli Molecular microbiology 60 1058 1075 10.1111/j.1365-2958.2006.05160.x 2006 16677314 · DOI
- [65]Rajagopalan S Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity Nature structural & molecular biology 20 740 747 10.1038/nsmb.2568 2013 PMC3676455 23644595 · DOI
- [67]Hattori M Mg(2+)-dependent gating of bacterial MgtE channel underlies Mg(2+) homeostasis The EMBO journal 28 3602 3612 10.1038/emboj.2009.288 2009 19798051 PMC2782099 · DOI · Paper page
- [68]Ma Z Faulkner MJ Helmann JD Origins of specificity and cross-talk in metal ion sensing by Bacillus subtilis Fur Molecular microbiology 86 1144 1155 10.1111/mmi.12049 2012 23057863 PMC3508374 · DOI · Paper page
- [69]Furukawa K Bacterial riboswitches cooperatively bind Ni(2+) or Co(2+) ions and control expression of heavy metal transporters Molecular cell 57 1088 1098 10.1016/j.molcel.2015.02.009 2015 25794617 PMC4667775 · DOI
- [70]Banerjee RV Johnston NL Sobeski JK Datta P Matthews RG Cloning and sequence analysis of the Escherichia coli metH gene encoding cobalamin-dependent methionine synthase and isolation of a tryptic fragment containing the cobalamin-binding domain The Journal of biological chemistry 264 13888 13895 1989 2668277
- [71]Nahvi A Genetic control by a metabolite binding mRNA Chemistry & biology 9 1043 2002 12323379
- [72]Rodionov DA Hebbeln P Gelfand MS Eitinger T Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters Journal of bacteriology 188 317 327 10.1128/jb.188.1.317-327.2006 2006 16352848 PMC1317602 · DOI
- [73]Gaballa A The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins Proceedings of the National Academy of Sciences of the United States of America 105 11927 11932 10.1073/pnas.0711752105 2008 18697947 PMC2575260 · DOI · Paper page
- [74]Masse E Gottesman S A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli Proceedings of the National Academy of Sciences of the United States of America 99 4620 4625 10.1073/pnas.032066599 2002 11917098 PMC123697 · DOI · Paper page
- [76]Yoch DC Valentine RC Ferredoxins and flavodoxins of bacteria Annual review of microbiology 26 139 162 10.1146/annurev.mi.26.100172.001035 1972 4562807 · DOI
- [77]Erdner DL Anderson DM Ferredoxin and flavodoxin as biochemical indicators of iron limitation during open-ocean iron enrichment Limnology and Oceanography 44 1609 1615 10.4319/lo.1999.44.7.1609 1999 · DOI
- [78]Smaldone GT A global investigation of the Bacillus subtilis iron-sparing response identifies major changes in metabolism Journal of bacteriology 194 2594 2605 10.1128/jb.05990-11 2012 22389480 PMC3347201 · DOI · Paper page
- [79]Masse E Arguin M Ironing out the problem: new mechanisms of iron homeostasis Trends Biochem Sci 30 462 468 10.1016/j.tibs.2005.06.005 2005 15996868 · DOI
- [80]Yost FJ Jr Fridovich I An iron-containing superoxide dismutase from Escherichia coli The Journal of biological chemistry 248 4905 4908 1973 4352182
- [81]Keele BB Jr McCord JM Fridovich I Superoxide dismutase from escherichia coli B. A new manganese-containing enzyme The Journal of biological chemistry 245 6176 6181 1970 4921969
- [82]Fee JA Regulation of sod genes in Escherichia coli: relevance to superoxide dismutase function Molecular microbiology 5 2599 2610 1991 1779751
- [83]Andrews SC Making DNA without iron - induction of a manganese-dependent ribonucleotide reductase in response to iron starvation Molecular microbiology 80 286 289 10.1111/j.1365-2958.2011.07594.x 2011 21371140 · DOI
- [84]Masse E Vanderpool CK Gottesman S Effect of RyhB small RNA on global iron use in Escherichia coli Journal of bacteriology 187 6962 6971 10.1128/jb.187.20.6962-6971.2005 2005 16199566 PMC1251601 · DOI
- [85]Mielcarek A Blauenburg B Miethke M Marahiel MA Molecular insights into frataxin-mediated iron supply for heme biosynthesis in Bacillus subtilis PloS one 10 e0122538 10.1371/journal.pone.0122538 2015 25826316 PMC4380498 · DOI
- [86]Gaballa A Wang T Ye RW Helmann JD Functional analysis of the Bacillus subtilis Zur regulon Journal of bacteriology 184 6508 6514 2002 12426338 PMC135443
- [87]Akanuma G Nanamiya H Natori Y Nomura N Kawamura F Liberation of zinc-containing L31 (RpmE) from ribosomes by its paralogous gene product, YtiA, in Bacillus subtilis Journal of bacteriology 188 2715 2720 10.1128/jb.188.7.2715-2720.2006 2006 16547061 PMC1428384 · DOI
- [88]Nanamiya H Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome Molecular microbiology 52 273 283 10.1111/j.1365-2958.2003.03972.x 2004 15049826 · DOI
- [89]Gabriel SE Helmann JD Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions Journal of bacteriology 191 6116 6122 10.1128/jb.00802-09 2009 19648245 PMC2747910 · DOI
- [90]Shin JH Helmann JD Molecular logic of the Zur-regulated zinc deprivation response in Bacillus subtilis Nature communications 7 12612 10.1038/ncomms12612 2016 PMC5007448 27561249 · DOI
- [91]Shin JH Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur Proceedings of the National Academy of Sciences of the United States of America 108 5045 5050 10.1073/pnas.1017744108 2011 21383173 PMC3064357 · DOI · Paper page
- [92]Gilston BA Structural and mechanistic basis of zinc regulation across the E. coli Zur regulon PLoS biology 12 e1001987 10.1371/journal.pbio.1001987 2014 25369000 PMC4219657 · DOI
- [93]Beauchene NA Impact of Anaerobiosis on Expression of the Iron-Responsive Fur and RyhB Regulons mBio 6 e01947 01915 10.1128/mBio.01947-15 2015 26670385 PMC4676285 · DOI
- [94]German N Doyscher D Rensing C Bacterial killing in macrophages and amoeba: do they all use a brass dagger? Future microbiology 8 1257 1264 10.2217/fmb.13.100 2013 24059917 · DOI
- [96]Ma Z Bacillithiol is a major buffer of the labile zinc pool in Bacillus subtilis Molecular microbiology 94 756 770 10.1111/mmi.12794 2014 25213752 PMC4227968 · DOI · Paper page
- [97]Newton GL Bacillithiol is an antioxidant thiol produced in Bacilli Nature chemical biology 5 625 627 10.1038/nchembio.189 2009 19578333 PMC3510479 · DOI
- [98]Sharma SV Chemical and Chemoenzymatic syntheses of bacillithiol: a unique low-molecular-weight thiol amongst low G + C Gram-positive bacteria Angewandte Chemie (International ed in English) 50 7101 7104 10.1002/anie.201100196 2011 21751306 · DOI
- [99]Helbig K Bleuel C Krauss GJ Nies DH Glutathione and transition-metal homeostasis in Escherichia coli Journal of bacteriology 190 5431 5438 10.1128/jb.00271-08 2008 18539744 PMC2493246 · DOI
- [100]Maret W Oxidative metal release from metallothionein via zinc-thiol/disulfide interchange Proceedings of the National Academy of Sciences of the United States of America 91 237 241 1994 8278372 PMC42922
- [101]Nairn BL The Response of Acinetobacter baumannii to Zinc Starvation Cell host & microbe 19 826 836 10.1016/j.chom.2016.05.007 2016 27281572 PMC4901392 · DOI · Paper page
- [103]Kay KL Hamilton CJ Le Brun NE Mass spectrometry of B. subtilis CopZ: Cu(i)-binding and interactions with bacillithiol Metallomics: integrated biometal science 8 709 719 10.1039/c6mt00036c 2016 27197762 · DOI
- [104]Potter AJ Trappetti C Paton JC Streptococcus pneumoniae uses glutathione to defend against oxidative stress and metal ion toxicity Journal of bacteriology 194 6248 6254 10.1128/jb.01393-12 2012 22984260 PMC3486410 · DOI
- [105]Culotta VC Daly MJ Manganese complexes: diverse metabolic routes to oxidative stress resistance in prokaryotes and yeast Antioxidants & redox signaling 19 933 944 10.1089/ars.2012.5093 2013 23249283 PMC3763226 · DOI · Paper page
- [106]Bruch EM Thomine S Tabares LC Un S Variations in Mn(II) speciation among organisms: what makes D. radiodurans different Metallomics: integrated biometal science 7 136 144 10.1039/c4mt00265b 2015 25407388 · DOI · Paper page
- [107]Sharma A Responses of Mn2+ speciation in Deinococcus radiodurans and Escherichia coli to gamma-radiation by advanced paramagnetic resonance methods Proceedings of the National Academy of Sciences of the United States of America 110 5945 5950 10.1073/pnas.1303376110 2013 23536297 PMC3625348 · DOI
- [108]Tabares LC Un S In situ determination of manganese(II) speciation in Deinococcus radiodurans by high magnetic field EPR: detection of high levels of Mn(II) bound to proteins The Journal of biological chemistry 288 5050 5055 10.1074/jbc.C112.444992 2013 23303180 PMC3576107 · DOI · Paper page
- [109]Tu WY Cellular iron distribution in Bacillus anthracis Journal of bacteriology 194 932 940 10.1128/jb.06195-11 2012 22178968 PMC3294808 · DOI · Paper page
- [110]Andrews SC Iron storage in bacteria Advances in microbial physiology 40 281 351 1998 9889981
- [111]Waidner B Essential role of ferritin Pfr in Helicobacter pylori iron metabolism and gastric colonization Infection and immunity 70 3923 3929 2002 12065536 PMC128114
- [112]Macedo S The nature of the di-iron site in the bacterioferritin from Desulfovibrio desulfuricans Nature structural biology 10 285 290 10.1038/nsb909 2003 12627224 · DOI
- [113]Carrondo MA Ferritins, iron uptake and storage from the bacterioferritin viewpoint The EMBO journal 22 1959 1968 10.1093/emboj/cdg215 2003 12727864 PMC156087 · DOI
- [114]Yang X Le Brun NE Thomson AJ Moore GR Chasteen ND The iron oxidation and hydrolysis chemistry of Escherichia coli bacterioferritin Biochemistry 39 4915 4923 2000 10769150
- [115]Kuberl A Polen T Bott M The pupylation machinery is involved in iron homeostasis by targeting the iron storage protein ferritin Proceedings of the National Academy of Sciences of the United States of America 113 4806 4811 10.1073/pnas.1514529113 2016 27078093 PMC4855571 · DOI
- [116]Beard SJ Hughes MN Poole RK Inhibition of the cytochrome bd-terminated NADH oxidase system in Escherichia coli K-12 by divalent metal cations FEMS microbiology letters 131 205 210 1995 7557331
- [117]Brekasis D Paget MS A novel sensor of NADH/NAD+ redox poise in Streptomyces coelicolor A3(2) The EMBO journal 22 4856 4865 10.1093/emboj/cdg453 2003 12970197 PMC212721 · DOI · Paper page
- [118]Alhasawi A Auger C Appanna VP Chahma M Appanna VD Zinc toxicity and ATP production in Pseudomonas fluorescens Journal of applied microbiology 117 65 73 10.1111/jam.12497 2014 24629129 · DOI
- [119]Chandrangsu P Helmann JD Intracellular Zn(II) Intoxication Leads to Dysregulation of the PerR Regulon Resulting in Heme Toxicity in Bacillus subtilis PLoS genetics 12 e1006515 10.1371/journal.pgen.1006515 2016 27935957 PMC5189952 · DOI
- [120]Shepherd M The cytochrome bd-I respiratory oxidase augments survival of multidrug-resistant Escherichia coli during infection Scientific reports 6 35285 10.1038/srep35285 2016 27767067 PMC5073308 · DOI
- [121]Mason MG Cytochrome bd confers nitric oxide resistance to Escherichia coli Nature chemical biology 5 94 96 10.1038/nchembio.135 2009 19109594 · DOI
- [122]Korshunov S Imlay KR Imlay JA The cytochrome bd oxidase of Escherichia coli prevents respiratory inhibition by endogenous and exogenous hydrogen sulfide Molecular microbiology 101 62 77 10.1111/mmi.13372 2016 26991114 PMC4925259 · DOI
- [124]Takeda H Structural basis for ion selectivity revealed by high-resolution crystal structure of Mg2+ channel MgtE Nature communications 5 5374 10.1038/ncomms6374 2014 PMC4241985 25367295 · DOI
- [125]Anjem A Imlay JA Mononuclear iron enzymes are primary targets of hydrogen peroxide stress The Journal of biological chemistry 287 15544 15556 10.1074/jbc.M111.330365 2012 22411989 PMC3346116 · DOI
- [126]Macomber L Imlay JA The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity Proceedings of the National Academy of Sciences of the United States of America 106 8344 8349 10.1073/pnas.0812808106 2009 19416816 PMC2688863 · DOI · Paper page
- [127]Xu FF Imlay JA Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli Applied and environmental microbiology 78 3614 3621 10.1128/aem.07368-11 2012 22344668 PMC3346352 · DOI
- [128]Chillappagari S Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis Journal of bacteriology 192 2512 2524 10.1128/jb.00058-10 2010 20233928 PMC2863568 · DOI
- [129]Martin JE Waters LS Storz G Imlay JA The Escherichia coli small protein MntS and exporter MntP optimize the intracellular concentration of manganese PLoS genetics 11 e1004977 10.1371/journal.pgen.1004977 2015 25774656 PMC4361602 · DOI
- [130]Begg SL Dysregulation of transition metal ion homeostasis is the molecular basis for cadmium toxicity in Streptococcus pneumoniae Nature communications 6 6418 10.1038/ncomms7418 2015 PMC4366526 25731976 · DOI
- [132]Faulkner MJ Ma Z Fuangthong M Helmann JD Derepression of the Bacillus subtilis PerR peroxide stress response leads to iron deficiency Journal of bacteriology 194 1226 1235 10.1128/jb.06566-11 2012 22194458 PMC3294777 · DOI · Paper page
- [133]Wakeman CA Menaquinone biosynthesis potentiates haem toxicity in Staphylococcus aureus Molecular microbiology 86 1376 1392 10.1111/mmi.12063 2012 23043465 PMC3524387 · DOI · Paper page
- [135]Damo SM Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens Proceedings of the National Academy of Sciences of the United States of America 110 3841 3846 10.1073/pnas.1220341110 2013 23431180 PMC3593839 · DOI · Paper page
- [138]Kapetanovic R Salmonella employs multiple mechanisms to subvert the TLR-inducible zinc-mediated antimicrobial response of human macrophages FASEB journal: official publication of the Federation of American Societies for Experimental Biology 30 1901 1912 10.1096/fj.201500061 2016 26839376 · DOI · Paper page
- [140]Francis MS Thomas CJ Mutants in the CtpA copper transporting P-type ATPase reduce virulence of Listeria monocytogenes Microbial pathogenesis 22 67 78 10.1006/mpat.1996.0092 1997 9049996 · DOI
- [141]Achard ME The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence Infection and immunity 78 2312 2319 10.1128/iai.01208-09 2010 20231415 PMC2863522 · DOI
- [143]McLaughlin HP A putative P-type ATPase required for virulence and resistance to haem toxicity in Listeria monocytogenes PloS one 7 e30928 10.1371/journal.pone.0030928 2012 22363518 PMC3283593 · DOI
- [144]Hubert K ZnuD, a potential candidate for a simple and universal Neisseria meningitidis vaccine Infection and immunity 81 1915 1927 10.1128/iai.01312-12 2013 23509142 PMC3676005 · DOI · Paper page
- [145]Anderson AS Staphylococcus aureus manganese transport protein C is a highly conserved cell surface protein that elicits protective immunity against S. aureus and Staphylococcus epidermidis The Journal of infectious diseases 205 1688 1696 10.1093/infdis/jis272 2012 22474033 PMC3348682 · DOI
- [146]Miyaji EN PsaA (pneumococcal surface adhesin A) and PspA (pneumococcal surface protein A) DNA vaccines induce humoral and cellular immune responses against Streptococcus pneumoniae Vaccine 20 805 812 2001 11738744
- [147]Keyer K Imlay JA Superoxide accelerates DNA damage by elevating free-iron levels Proceedings of the National Academy of Sciences of the United States of America 93 13635 13640 1996 8942986 PMC19375
- [148]Irving H Williams RJP 637. The stability of transition-metal complexes Journal of the Chemical Society (Resumed) 3192 3210 10.1039/JR9530003192 1953 · DOI · Paper page
- [149]Foster AW Osman D Robinson NJ Metal preferences and metallation The Journal of biological chemistry 289 28095 28103 10.1074/jbc.R114.588145 2014 25160626 PMC4192464 · DOI
- [150]Braymer JJ Giedroc DP Recent developments in copper and zinc homeostasis in bacterial pathogens Curr Opin Chem Biol 19 59 66 10.1016/j.cbpa.2013.12.021 2014 24463765 PMC4008645 · DOI · Paper page
- [151]Outten FW Huffman DL Hale JA O’Halloran TV The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli The Journal of biological chemistry 276 30670 30677 10.1074/jbc.M104122200 2001 11399769 · DOI
- [152]Rensing C McDevitt SF The copper metallome in prokaryotic cells Metal ions in life sciences 12 417 450 10.1007/978-94-007-5561-1_12 2013 23595679 · DOI
- [153]Maguire ME Cowan JA Magnesium chemistry and biochemistry Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine 15 203 210 2002 12206387
- [154]Helmann JD Specificity of metal sensing: iron and manganese homeostasis in Bacillus subtilis The Journal of biological chemistry 289 28112 28120 10.1074/jbc.R114.587071 2014 25160631 PMC4192466 · DOI · Paper page
- [155]Lemire JA Harrison JJ Turner RJ Antimicrobial activity of metals: mechanisms, molecular targets and applications Nature reviews. Microbiology 11 371 384 10.1038/nrmicro3028 2013 23669886 · DOI
- [156]Tottey S Cyanobacterial metallochaperone inhibits deleterious side reactions of copper Proceedings of the National Academy of Sciences of the United States of America 109 95 100 10.1073/pnas.1117515109 2012 22198771 PMC3252907 · DOI
- [157]Guedon E Helmann JD Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators Molecular microbiology 48 495 506 2003 12675807
- [158]Cavet JS A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity The Journal of biological chemistry 277 38441 38448 10.1074/jbc.M207677200 2002 12163508 · DOI
- [159]Harvie DR Predicting metals sensed by ArsR-SmtB repressors: allosteric interference by a non-effector metal Molecular microbiology 59 1341 1356 10.1111/j.1365-2958.2006.05029.x 2006 16430705 · DOI
- [160]Ma Z Cowart DM Scott RA Giedroc DP Molecular insights into the metal selectivity of the copper(I)-sensing repressor CsoR from Bacillus subtilis Biochemistry 48 3325 3334 10.1021/bi900115w 2009 19249860 PMC2728441 · DOI
- [161]Dalmas O Sompornpisut P Bezanilla F Perozo E Molecular mechanism of Mg2+-dependent gating in CorA Nature communications 5 3590 10.1038/ncomms4590 2014 PMC4066822 24694723 · DOI
- [162]Hattori M Tanaka Y Fukai S Ishitani R Nureki O Crystal structure of the MgtE Mg2+ transporter Nature 448 1072 1075 10.1038/nature06093 2007 17700703 · DOI
- [163]Zhao H Eide D The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation Proceedings of the National Academy of Sciences of the United States of America 93 2454 2458 1996 8637895 PMC39818
- [164]MacDiarmid CW Milanick MA Eide DJ Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock The Journal of biological chemistry 278 15065 15072 10.1074/jbc.M300568200 2003 12556516 · DOI
- [165]Knutson MD Oukka M Koss LM Aydemir F Wessling-Resnick M Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin Proceedings of the National Academy of Sciences of the United States of America 102 1324 1328 10.1073/pnas.0409409102 2005 15665091 PMC547844 · DOI · Paper page
- [166]Stafford SL Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper Bioscience reports 33 10.1042/bsr20130014 2013 PMC3712485 23738776 · DOI
- [167]Raimunda D Long JE Sassetti CM Arguello JM Role in metal homeostasis of CtpD, a Co(2)(+) transporting P(1B4)-ATPase of Mycobacterium smegmatis Molecular microbiology 84 1139 1149 10.1111/j.1365-2958.2012.08082.x 2012 22591178 PMC3370075 · DOI
- [168]Hao X Survival in amoeba--a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a “copper pathogenicity island” Applied microbiology and biotechnology 99 5817 5824 10.1007/s00253-015-6749-0 2015 26088177 · DOI
- [169]Buracco S Dictyostelium Nramp1, which is structurally and functionally similar to mammalian DMT1 transporter, mediates phagosomal iron efflux Journal of cell science 128 3304 3316 10.1242/jcs.173153 2015 26208637 PMC4582194 · DOI
- [170]Peracino B Buracco S Bozzaro S The Nramp (Slc11) proteins regulate development, resistance to pathogenic bacteria and iron homeostasis in Dictyostelium discoideum Journal of cell science 126 301 311 10.1242/jcs.116210 2013 22992462 · DOI
- [171]Burlando B Occurrence of Cu-ATPase in Dictyostelium: possible role in resistance to copper Biochemical and biophysical research communications 291 476 483 10.1006/bbrc.2002.6463 2002 11855813 · DOI
- [172]Hao X A role for copper in protozoan grazing - two billion years selecting for bacterial copper resistance Molecular microbiology 10.1111/mmi.13483 2016 27528008 · DOI
- [173]Fields BS The molecular ecology of legionellae Trends in microbiology 4 286 290 1996 8829338
- [174]Hilbi H Segal G Shuman HA Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila Molecular microbiology 42 603 617 2001 11722729
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- Authors
- Chandrangsu, P., Rensing, C., & Helmann, J. D.
- Affiliations
- Cornell University (US)
- J. Craig Venter Institute (US)
- Corresponding author
- Rensing, Christopher
- Helmann, John D.
- Venue
- Nature Reviews Microbiology
- Published
- 2017-03-27
- Volume
- 15
- Issue
- 6
- Pages
- 338-350
- ISSN
- 1740-1526 (ISSN-L)
- 1740-1534
- PMC
- PMC5963929
- OpenAlex
- W2597506409
- Cited by
- 812
- References
- 23
- Citations by year
- 2026: 133 · 2025: 96 · 2024: 94 · 2023: 94 · 2022: 111 · 2021: 86 · 2020: 78 · 2019: 61 · 2018: 46 · 2017: 12
- FWCI
- 6.98
- Type
- journal article
- Language
- en
- Update notices
- erratum (2017-06-01)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Reviews Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM059323)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Keywords
- metal homeostasis, metal limitation, metal toxicity, host-pathogen interaction, metal efflux, metal storage, metal imports, metal cofactors, post-transcriptional regulation
- MeSH terms
- Bacillus subtilis, Bacterial Proteins, Iron, Manganese, Membrane Proteins, Repressor Proteins, Zinc, Riboswitch
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