Characterization of the response to zinc deficiency in the cyanobacterium Anabaena sp. strain PCC 7120

Journal of Bacteriology

Volumn 194, Issue 10, 2012, Pages 2426-2436

  Napolitano, Mauro ^a   Rubio, Miguel Ángel ^a   Santamaría Gómez, Javier ^a   Olmedo Verd, Elvira ^a,c   Robinson, Nigel J ^b   Luque, Ignacio ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b DURHAM UNIVERSITY   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; DNA; METALLOCHAPERONE; METALLOPROTEIN; PROTEIN TONB; UNCLASSIFIED DRUG; ZINC; ZUR PROTEIN;

ANABAENA; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DNA BINDING; GENE CLUSTER; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE SEQUENCE; HOMEOSTASIS; MEMBRANE TRANSPORT; NONHUMAN; OPEN READING FRAME; OPERON; OUTER MEMBRANE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; REGULON; ZINC DEFICIENCY;

ANABAENA; BACTERIAL PROTEINS; BASE SEQUENCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; METALLOPROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; ZINC;

ANABAENA; ANABAENA SP.;

EID: 84861361870     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00090-12     Document Type: Article

References (63)

1. Ausubel FM, et al. 2010. Current protocols in molecular biology. Greene Publishing & Wiley-Interscience, New York, NY.
2. Baichoo N, Helmann JD. 2002. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J. Bacteriol. 184:5826-5832.
3. Baichoo N, Wang T, Ye R, Helmann JD. 2002. Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol. Microbiol. 45:1613-1629.
4. Bensing BA, Meyer BJ, Dunny GM. 1996. Sensitive detection of bacterial transcription initiation sites and differentiation from RNA processing sites in the pheromone-induced plasmid transfer system of Enterococcus faecalis. Proc. Natl. Acad. Sci. U. S. A. 93:7794-7799.
5. Blaby-Haas CE, Furman R, Rodionov DA, Artsimovitch I, de Crecy-Lagard V. 2011. Role of a Zn-independent DksA in Zn homeostasis and stringent response. Mol. Microbiol. 79:700-715.
6. Blindauer CA, Razi MT, Parsons S, Sadler PJ. 2006. Metal complexes of N, N, N', N'-tetrakis(2-pyridylmethyl)ethylenediamine (TPEN): variable coordination numbers and geometries. Polyhedron 25:513-520.
7. Blindauer CA. 2008. Zinc-handling in cyanobacteria: an update. Chem. Biodivers. 5:1990-2013.
8. Blindauer CA, et al. 2002. Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol. Microbiol. 45:1421-1432.
9. Borrelly GP, Rondet SA, Tottey S, Robinson NJ. 2004. Chimeras of P-type ATPases and their transcriptional regulators: contributions of a cytosolic amino-terminal domain to metal specificity. Mol. Microbiol. 53:217-227.
10. Brocklehurst KR, et al. 1999. ZntR is a Zn(II)-responsive MerR-like transcriptional regulator of zntA in Escherichia coli. Mol. Microbiol. 31: 893-902.
11. Capone DG, Zehr J, Paerl HW, Bergman B, Carpenter EJ. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221-1229.
12. Cavet JS, Borrelly GP, Robinson NJ. 2003. Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol. Rev. 27:165-181.
13. Coleman JE. 1992. Zinc proteins: enzymes, storage proteins, transcription factors, and replication proteins. Annu. Rev. Biochem. 61:897-946.
14. Elhai J, Wolk CP. 1988. Conjugal transfer of DNA to cyanobacteria. Methods Enzymol. 167:747-754.
15. Elhai J, Wolk CP. 1988. A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers. Gene 68:119-138.
16. El Yacoubi B, et al. 2006. Discovery of a new prokaryotic type I GTP cyclohydrolase family. J. Biol. Chem. 281:37586-37593.
17. Escolar L, Perez-Martin J, de Lorenzo V. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181: 6223-6229.
18. Feng Y, et al. 2008. Functional definition and global regulation of Zur, a zinc uptake regulator in a Streptococcus suis serotype 2 strain causing streptococcal toxic shock syndrome. J. Bacteriol. 190:7567-7578.
19. Gaballa A, Helmann JD. 1998. Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J. Bacteriol. 180:5815-5821.
20. Gaballa A, Wang T, Ye RW, Helmann JD. 2002. Functional analysis of the Bacillus subtilis Zur regulon. J. Bacteriol. 184:6508-6514.
21. Gabriel SE, Helmann JD. 2009. Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J. Bacteriol. 191:6116-6122.
22. Gabriel SE, Miyagi F, Gaballa A, Helmann JD. 2008. Regulation of the Bacillus subtilis yciC gene and insights into the DNA-binding specificity of the zinc-sensing metalloregulator Zur. J. Bacteriol. 190:3482-3488.
23. Goericke R, Welshmeyer NA. 1993. The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res. 40:2283-2294.
24. Haas CE, et al. 2009. A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 10:470.
25. Haft DH, Paulsen IT, Ward N, Selengut JD. 2006. Exopolysaccharideassociated protein sorting in environmental organisms: the PEP-CTERM/ EpsH system. Application of a novel phylogenetic profiling heuristic. BMC Biol. 4:29.
26. Hantke K. 2005. Bacterial zinc uptake and regulators. Curr. Opin. Microbiol. 8:196-202.
27. Hernández JA, López-Gomollón S, Bes MT, Fillat MF, Peleato ML. 2004. Three fur homologues from Anabaena sp. PCC7120: exploring reciprocal protein-promoter recognition. FEMS Microbiol. Lett. 236:275-282.
28. Higgins CF. 2001. ABC transporters: physiology, structure and mechanism-an overview. Res. Microbiol. 152:205-210.
29. Hohle TH, Franck WL, Stacey G, O'Brian MR. 2011. Bacterial outer membrane channel for divalent metal ion acquisition. Proc. Natl. Acad. Sci. U. S. A. 108:15390-15395.
30. Hudek L, et al. 2009. Bioinformatic and expression analyses of genes mediating zinc homeostasis in Nostoc punctiforme. Appl. Environ. Microbiol. 75:784-791.
31. Jaffe EK. 2003. An unusual phylogenetic variation in the metal ion binding sites of porphobilinogen synthase. Chem. Biol. 10:25-34.
32. Kloosterman TG, van der Kooi-Pol MM, Bijlsma JJ, Kuipers OP. 2007. The novel transcriptional regulator SczA mediates protection against Zn2+stress by activation of the Zn2+resistance gene czcD in Streptococcus pneumoniae. Mol. Microbiol. 65:1049-1063.
33. Lee JW, Helmann JD. 2007. Functional specialization within the Fur family of metalloregulators. Biometals 20:485-499.
34. Li Y, et al. 2009. Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol. 9:128.
35. Liu HB, Nolla HA, Campbell L. 1997. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquatic Microb. Ecol. 12:39-47.
36. Liu T, Golden JW, Giedroc DP. 2005. A zinc(II)/lead(II)/cadmium(II)-inducible operon from the cyanobacterium Anabaena is regulated by AztR, an alpha3N ArsR/SmtB metalloregulator. Biochemistry 44:8673-8683.
37. Llull D, et al. 2011. Lactococcus lactis ZitR is a zinc-responsive repressor active in the presence of low, nontoxic zinc concentrations in vivo. J. Bacteriol. 193:1919-1929.
38. López-Gomollón S, Sevilla E, Bes MT, Peleato ML, Fillat MF. 2009. New insights into the role of Fur proteins: FurB (All2473) from Anabaena protects DNA and increases cell survival under oxidative stress. Biochem. J. 418:201-207.
39. Lucarelli D, et al. 2007. Crystal structure and function of the zinc uptake regulator FurB from Mycobacterium tuberculosis. J. Biol. Chem. 282: 9914-9922.
40. Luque I, Contreras A, Zabulon G, Herrero A, Houmard J. 2002. Expression of the glutamyl-tRNA synthetase gene from the cyanobacterium Synechococcus sp PCC 7942 depends on nitrogen availability and the global regulator NtcA. Mol. Microbiol. 46:1157-1167.
41. Ma Z, Gabriel SE, Helmann JD. 2011. Sequential binding and sensing of Zn(II) by Bacillus subtilis Zur. Nucleic Acids Res. 39:9130-9138.
42. Maciag A, et al. 2007. Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J. Bacteriol. 189:730-740.
43. Mirus O, Strauss S, Nicolaisen K, von Haeseler A, Schleiff E. 2009. TonB-dependent transporters and their occurrence in cyanobacteria. BMC Biol. 7:68.
44. Noinaj N, Guillier M, Barnard TJ, Buchanan SK. 2010. TonB-dependent transporters: regulation, structure, and function. Annu. Rev. Microbiol. 64:43-60.
45. Outten CE, O'Halloran TV. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488-2492.
46. Panina EM, Mironov AA, Gelfand MS. 2003. Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. U. S. A. 100:9912-9917.
47. Partensky F, Hess WR, Vaulot D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63:106-127.
48. Rippka R. 1988. Isolation and purification of cyanobacteria. Methods Enzymol. 167:3-27.
49. Robinson NJ, et al. 1990. Prokaryotic metallothionein gene characterization and expression: chromosome crawling by ligation-mediated PCR. Proc. Biol. Sci. 242:241-247.
50. Sankaran B, et al. 2009. Zinc-independent folate biosynthesis: genetic, biochemical, and structural investigations reveal new metal dependence for GTP cyclohydrolase IB. J. Bacteriol. 191:6936-6949.
51. Schauer K, Gouget B, Carriere M, Labigne A, de Reuse H. 2007. Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol. Microbiol. 63:1054-1068.
52. Schroder J, Jochmann N, Rodionov DA, Tauch A. 2010. The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 11:12.
53. Segel IH. 1976. Biochemical calculations, 2nd ed. John Wiley and Sons, Inc, New York, NY.
54. 2+limitation and the repressor/ activator function of AdcR. Metallomics 3:609-618.
55. Shin JH, 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.
56. Sigdel TK, Easton JA, Crowder MW. 2006. Transcriptional response of Escherichia coli to TPEN. J. Bacteriol. 188:6709-6713.
57. Smith KS, Ferry JG. 2000. Prokaryotic carbonic anhydrases. FEMS Microbiol. Rev. 24:335-366.
58. Stork M, et al. 2010. An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog. 6:e1000969.
59. Tottey S, et al. 2012. Cyanobacterial metallochaperone inhibits deleterious side reactions of copper. Proc. Natl. Acad. Sci. U. S. A. 109:95-100.
60. Vioque A. 1992. Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucleic Acids Res. 20:6331-6337.
61. Waldron KJ, Robinson NJ. 2009. How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 7:25-35.
62. Whitton BA, Potts M. 2002. Introduction to the cyanobacteria, p 1-10. In Whitton BA, PottsM(ed), The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publisher, New York, NY.
63. Yu NY, et al. 2010. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608-1615.