Transport of Magnesium by a Bacterial Nramp-Related Gene

English version České info

Magnesium ions are essential for life, and, correspondingly, all organisms must encode for proteins to transport them. Three classes of bacterial proteins (CorA, MgtE and MgtA/B) have previously been identified for transport of the ion. This current study introduces a new route of magnesium import, which, moreover, is unexpectedly provided by proteins distantly related to Natural resistance-associated macrophage proteins (Nramp). Nramp metal transporters are widespread in the three domains of life; however, most are assumed to function as transporters of transition metals such as manganese or iron. None of the previously characterized Nramps have been shown to transport magnesium. In this study, we demonstrate that certain bacterial proteins, distantly related to Nramp homologues, exhibit transport of magnesium. We also find that these new magnesium transporters are genetically controlled by a magnesium-sensing regulatory element. Importantly, we find numerous additional examples of similar genes sharing this regulatory arrangement, suggesting that these genes may be a frequent occurrence in bacteria, and may represent a class of magnesium transporters. Therefore, our aggregate data discover a new and perhaps broadly important path of magnesium import in bacteria.

Vyšlo v časopise: Transport of Magnesium by a Bacterial Nramp-Related Gene. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004429
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004429

Souhrn

Zdroje

1. AndreiniC, BertiniI, CavallaroG, HollidayGL, ThorntonJM (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13: 1205–1218 doi:10.1007/s00775-008-0404-5

2. WaldronKJ, RutherfordJC, FordD, RobinsonNJ (2009) Metalloproteins and metal sensing. Nature 460: 823–830 doi:10.1038/nature08300

3. GuerraAJ, GiedrocDP (2012) Metal site occupancy and allosteric switching in bacterial metal sensor proteins. Arch Biochem Biophys 519: 210–222 doi:10.1016/j.abb.2011.11.021

4. MooreCM, HelmannJD (2005) Metal ion homeostasis in Bacillus subtilis. Curr Opin Microbiol 8: 188–195 doi:10.1016/j.mib.2005.02.007

5. PennellaMA, GiedrocDP (2005) Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. Biometals 18: 413–428 doi:10.1007/s10534-005-3716-8

6. GiedrocDP, ArunkumarAI (2007) Metal sensor proteins: nature's metalloregulated allosteric switches. Dalton Trans 63: 3107–3120 doi:10.1039/b706769k

7. SkameneE, GrosP, ForgetA, KongshavnPAL, St CharlesC, et al. (1982) Genetic regulation of resistance to intracellular pathogens. Nature 297: 506–509 doi:10.1038/297506a0

8. HuJ, BumsteadN, BarrowP, SebastianiG, OlienL, et al. (1997) Resistance to salmonellosis in the chicken is linked to NRAMP1 and TNC. Genome Res 7: 693–704 doi:10.1101/gr.7.7.693

9. LangT, PrinaE, SibthorpeD, BlackwellJM (1997) Nramp1 transfection transfers Ity/Lsh/Bcg-related pleiotropic effects on macrophage activation: influence on antigen processing and presentation. Infect Immun 65: 380–386.

10. PinnerE, GruenheidS, RaymondM, GrosP (1997) Functional complementation of the yeast divalent cation transporter family SMF by NRAMP2, a member of the mammalian natural resistance-associated macrophage protein family. J Biol Chem 272: 28933–28938 doi:10.1074/jbc.272.46.28933

11. SupekF, SupekovaL, NelsonH, NelsonN (1997) Function of metal-ion homeostasis in the cell division cycle, mitochondrial protein processing, sensitivity to mycobacterial infection and brain function. J Exp Biol 200: 321–330.

12. ZwillingBS, KuhnDE, WikoffL, BrownD, LafuseW (1999) Role of iron in Nramp1-mediated inhibition of mycobacterial growth. Infect Immun 67: 1386–1392.

13. GomesMS, AppelbergR (1998) Evidence for a link between iron metabolism and Nramp1 gene function in innate resistance against Mycobacterium avium. Immunology 95: 165–168.

14. BoechatN, BordatY, RauzierJ, HanceAJ, GicquelB, et al. (2002) Disruption of the Gene Homologous to Mammalian Nramp1 in Mycobacterium tuberculosis Does Not Affect Virulence in Mice. 70: 4124–4131 doi:10.1128/IAI.70.8.4124

15. DomenechP, PymAS, CellierM, BarryCE, ColeST (2002) Inactivation of the Mycobacterium tuberculosis Nramp orthologue (mntH) does not affect virulence in a mouse model of tuberculosis. FEMS Microbiol Lett 207: 81–86.

16. GovoniG, GrosP (1998) Macrophage NRAMP1 and its role in resistance to microbial infections. Inflamm Res 47: 277–284 doi:10.1007/s000110050330

17. NelsonN (1999) Metal ion transporters and homeostasis. EMBO J 18: 4361–4371.

18. ForbesJR, GrosP (2003) Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 102: 1884–1892 doi:10.1182/blood-2003-02-0425

19. ForbesJR, GrosP (2001) Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol 9: 397–403 doi:10.1016/S0966-842X(01)02098-4

20. KehresDG, ZaharikML, FinlayBB, MaguireME (2000) The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36: 1085–1100 doi:[]mmi1922 [pii]

21. GunshinH, MackenzieB, Berger UV, GunshinY, RomeroMF, et al. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482–488 doi:10.1038/41343

22. MakuiH, RoigE, ColeST, HelmannJD, GrosP, et al. (2000) Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35: 1065–1078.

23. RomaniAM, ScarpaA (2000) Regulation of cellular magnesium. Front Biosci 5: D720–D734 doi:10.2741/Romani

24. MoomawAS, MaguireME (2008) The unique nature of mg2+ channels. Physiol Bethesda Md 23: 275–285.

25. ReinhartRA (1988) Magnesium metabolism. A review with special reference to the relationship between intracellular content and serum levels. Arch Intern Med 148: 2415–2420 doi:10.1001/archinte.1988.00380110065013

26. ChenK, YuldashevaS, Penner-HahnJE, O'HalloranTV (2003) An atypical linear Cu(I)-S2 center constitutes the high-affinity metal-sensing site in the CueR metalloregulatory protein. J Am Chem Soc 125: 12088–12089 doi:10.1021/ja036070y

27. ChiversPT, SauerRT (2000) Regulation of high affinity nickel uptake in bacteria. Ni2+-Dependent interaction of NikR with wild-type and mutant operator sites. J Biol Chem 275: 19735–19741 doi:10.1074/jbc.M002232200

28. ShinJ-H, JungHJ, AnYJ, ChoY-B, ChaS-S, et al. (2011) Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur. Proc Natl Acad Sci U S A 108: 5045–5050.

29. GrubbsRD, MaguireME (1987) Magnesium as a regulatory cation: criteria and evaluation. Magnesium 6: 113–127.

30. WilliamsRJ (1970) Cation distributions and the energy status of cells. J Bioenerg 1: 215–225.

31. FlatmanPW (1991) Mechanisms of magnesium transport. Annu Rev Physiol 53: 259–271 doi:10.1146/annurev.ph.53.030191.001355

32. FroschauerEM, KolisekM, DieterichF, SchweigelM, SchweyenRJ (2004) Fluorescence measurements of free [Mg2+] by use of mag-fura 2 in Salmonella enterica. FEMS Microbiol Lett 237: 49–55.

33. MaguireME (2006) The structure of CorA: a Mg(2+)-selective channel. Curr Opin Struct Biol 16: 432–438 doi:10.1016/j.sbi.2006.06.006

34. GardnerRC (2003) Genes for magnesium transport. Curr Opin Plant Biol 6: 263–267 doi:10.1016/S1369-5266(03)00032-3

35. HmielSP, SnavelyMD, FlorerJB, MaguireME, MillerCG (1989) Magnesium transport in Salmonella typhimurium: genetic characterization and cloning of three magnesium transport loci. J Bacteriol 171: 4742–4751.

36. KehresDG, MaguireME (2002) Structure, properties and regulation of magnesium transport proteins. Biometals 15: 261–270.

37. SmithRL, MaguireME (1995) Distribution of the CorA Mg2+ transport system in gram-negative bacteria. J Bacteriol 177: 1638–1640.

38. SmithRL, MaguireME (1998) Microbial magnesium transport: unusual transporters searching for identity. Mol Microbiol 28: 217–226.

39. PerezJC, ShinD, ZwirI, LatifiT, HadleyTJ, et al. (2009) Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet 5: e1000428.

40. CromieMJ, ShiY, LatifiT, GroismanEA (2006) An RNA sensor for intracellular Mg(2+). Cell 125: 71–84 doi:10.1016/j.cell.2006.01.043

41. DannCE, WakemanCA, SielingCL, BakerSC, IrnovI, et al. (2007) Structure and mechanism of a metal-sensing regulatory RNA. Cell 130: 878–892 doi:10.1016/j.cell.2007.06.051

42. RameshA, WinklerWC (2010) Magnesium-sensing riboswitches in bacteria. RNA Biol 7: 77–83 doi:10.4161/rna.7.1.10490

43. WakemanCA, WinklerWC, DannCE (2007) Structural features of metabolite-sensing riboswitches. Trends Biochem Sci 32: 415–424.

44. NudlerE, MironovA, NudlerE, MironovAS (2004) The riboswitch control of bacterial metabolism. Trends Biochem Sci 29: 11–17 doi:10.1016/j.tibs.2003.11.004

45. SchwalbeH, BuckJ, FürtigB, NoeskeJ, WöhnertJ (2007) Structures of RNA switches: insight into molecular recognition and tertiary structure. Angew Chem Int Ed Engl 46: 1212–1219 doi:10.1002/anie.200604163

46. MontangeRK, BateyRT (2008) Riboswitches: emerging themes in RNA structure and function. Annu Rev Biophys 37: 117–133 doi:10.1146/annurev.biophys.37.032807.130000

47. DambachMD, WinklerWC (2009) Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12: 161–169.

48. RothA, BreakerRR (2009) The structural and functional diversity of metabolite-binding riboswitches. Annu Rev Biochem 78: 305–334 doi:10.1146/annurev.biochem.78.070507.135656

49. RameshA, WakemanCA, WinklerWC (2011) Insights into metalloregulation by M-box riboswitch RNAs via structural analysis of manganese-bound complexes. J Mol Biol 407: 556–570.

50. WakemanCA, RameshA, WinklerWC (2009) Multiple metal-binding cores are required for metalloregulation by M-box riboswitch RNAs. J Mol Biol 392: 723–735.

51. BarrickJE (2009) Predicting riboswitch regulation on a genomic scale. Methods Mol Biol 540: 1–13 doi:_10.1007/978-1-59745-558-9_1

52. JakubovicsNS, JenkinsonHF (2001) Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147: 1709–1718.

53. QueQ, HelmannJD (2000) Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Mol Microbiol 35: 1454–1468.

54. KehresDG, JanakiramanA, SlauchJM, MaguireME (2002) Regulation of Salmonella enterica serovar Typhimurium mntH transcription by H(2)O(2), Fe(2+), and Mn(2+). J Bacteriol 184: 3151–3158.

55. RicherE, CourvilleP, BergevinI, CellierMFM (2003) Horizontal gene transfer of “prototype” Nramp in bacteria. J Mol Evol 57: 363–376 doi:10.1007/s00239-003-2472-z

56. HohleTH, O'BrianMR (2009) The mntH gene encodes the major Mn(2+) transporter in Bradyrhizobium japonicum and is regulated by manganese via the Fur protein. Mol Microbiol 72: 399–409.

57. WakemanCA, GoodsonJR, ZachariaVM, WinklerWC (2014) An Assessment of the Requirements for Magnesium Transporters in Bacillus subtilis. J Bacteriol 196(6): 1206–14 doi:10.1128/JB.01238-13

58. CellierMF, BergevinI, BoyerE, RicherE (2001) Polyphyletic origins of bacterial Nramp transporters. Trends Genet 17: 365–370 doi:10.1016/S0168-9525(01)02364-2

59. ChaloupkaR, CourvilleP, VeyrierF, KnudsenB, Tompkins Ta, et al. (2005) Identification of functional amino acids in the Nramp family by a combination of evolutionary analysis and biophysical studies of metal and proton cotransport in vivo. Biochemistry 44: 726–733 doi:10.1021/bi048014v

60. Cellier M, Gros P (2004) The Nramp Family. Georgetown: Eurekah.com.

61. CourvilleP, UrbankovaE, RensingC, ChaloupkaR, QuickM, et al. (2008) Solute carrier 11 cation symport requires distinct residues in transmembrane helices 1 and 6. J Biol Chem 283: 9651–9658 doi:10.1074/jbc.M709906200

62. CellierMFM (2012) Nutritional immunity: homology modeling of Nramp metal import. Adv Exp Med Biol 946: 335–351 doi:_10.1007/978-1-4614-0106-3_19

63. TownsendDE, EsenwineAJ, GeorgeJ, BrossD, MaguireME, et al. (1995) Cloning of the mgtE Mg2+ transporter from Providencia stuartii and the distribution of mgtE in gram-negative and gram-positive bacteria. J Bacteriol 177: 5350–5354.

64. SmithRL, BanksJL, SnavelyMD, MaguireME (1993) Sequence and topology of the CorA magnesium transport systems of Salmonella typhimurium and Escherichia coli. Identification of a new class of transport protein. J Biol Chem 268: 14071–14080.

65. TaoT, SnavelyMD, FarrSG, MaguireME (1995) Magnesium transport in Salmonella typhimurium: mgtA encodes a P-type ATPase and is regulated by Mg2+ in a manner similar to that of the mgtB P-type ATPase. J Bacteriol 177: 2654–2662.

66. AgranoffD, MonahanIM, ManganJA, ButcherPD, KrishnaS (1999) Mycobacterium tuberculosis expresses a novel pH-dependent divalent cation transporter belonging to the Nramp family. J Exp Med 190: 717–724.

67. CzachorowskiM, Lam-Yuk-TseungS, CellierM, GrosP (2009) Transmembrane topology of the mammalian Slc11a2 iron transporter. Biochemistry 48: 8422–8434 doi:10.1021/bi900606y

68. AnagnostopoulosC, SpizizenJ (1961) Requirements for transformation in Bacillus subtilis. J Bacteriol 81: 741–746.

69. Van OoijC, LosickR (2003) Subcellular localization of a small sporulation protein in Bacillus subtilis. J Bacteriol 185: 1391–1398.

70. ArnaudM, ChastanetA, DébarbouilléM (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887–6891 doi:10.1128/AEM.70.11.6887-6891.2004

71. ZhangH, DavisonW, MillerS, TychW (1995) In situ high resolution measurements of fluxes of Ni, Cu, Fe, and Mn and concentrations of Zn and Cd in porewaters by DGT. Geochim Cosmochim Acta 59: 4181–4192 doi:10.1016/0016-7037(95)00293-9

72. TobinMB, PeeryRB, SkatrudPL (1997) Genes encoding multiple drug resistance-like proteins in Aspergillus fumigatus and Aspergillus flavus. Gene 200: 11–23 doi:10.1016/S0378-1119(97)00281-3

73. DeikusG, BabitzkeP, BechhoferDH (2004) Recycling of a regulatory protein by degradation of the RNA to which it binds. Proc Natl Acad Sci U S A 101: 2747–2751.

74. RoosJW, McLaughlinJK, PapoutsakisET (1985) The effect of pH on nitrogen supply, cell lysis, and solvent production in fermentations of Clostridium acetobutylicum. Biotechnol Bioeng 27: 681–694 doi:10.1002/bit.260270518

75. KatohK, StandleyDM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780 doi:10.1093/molbev/mst010

76. RonquistF, HuelsenbeckJP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574 doi:10.1093/bioinformatics/btg180

77. AltekarG, DwarkadasS, HuelsenbeckJP, RonquistF (2004) Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407–415 doi:10.1093/bioinformatics/btg427

78. HelaersR, MilinkovitchMC (2010) MetaPIGA v2.0: maximum likelihood large phylogeny estimation using the metapopulation genetic algorithm and other stochastic heuristics. BMC Bioinformatics 11: 379 doi:10.1186/1471-2105-11-379

79. TamuraK, StecherG, PetersonD, FilipskiA, KumarS (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725–2729 doi:10.1093/molbev/mst197