Home LiteratureArticle Details
PMID: 12949088 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803.

Journal of bacteriology ·Vol. 185 ·No. 18 ·2003-09-00 ·Pages 5363-71

López-Maury L, Florencio FJ, Reyes JC

Abstract

Arsenic is one of the most important global environmental pollutants. Here we show that the cyanobacterium Synechocystis sp. strain PCC 6803 contains an arsenic and antimony resistance operon consisting of three genes: arsB, encoding a putative arsenite and antimonite carrier, arsH, encoding a protein of unknown function, and arsC, encoding a putative arsenate reductase. While arsB mutant strains were sensitive to arsenite, arsenate, and antimonite, arsC mutants were sensitive only to arsenate. The arsH mutant strain showed no obvious phenotype under the conditions tested. In vivo the arsBHC operon was derepressed by oxyanions of arsenic and antimony (oxidation state, +3) and, to a lesser extent, by bismuth (oxidation state, +3) and arsenate (oxidation state, +5). In the absence of these effectors, the operon was repressed by a transcription repressor of the ArsR/SmtB family, encoded by an unlinked gene termed arsR. Thus, arsR null mutants showed constitutive derepression of the arsBHC operon. Expression of the arsR gene was not altered by the presence of arsenic or antimony compounds. Purified recombinant ArsR protein binds to the arsBHC promoter-operator region in the absence of metals and dissociates from the DNA in the presence of Sb(III) or As(III) but not in the presence of As(V), suggesting that trivalent metalloids are the true inducers of the system. DNase I footprinting experiments indicate that ArsR binds to two 17-bp direct repeats, with each one consisting of two inverted repeats, in the region from nucleotides -34 to + 17 of the arsBHC promoter-operator.

MeSH Terms
Antimony/pharmacology Arsenic/pharmacology,physiology Arsenite Transporting ATPases Bacterial Proteins Base Sequence Binding Sites Bismuth/pharmacology Chemotaxis/physiology Cyanobacteria/drug effects,physiology DNA-Binding Proteins/genetics,metabolism Drug Resistance, Bacterial/physiology Gene Expression Regulation, Bacterial/drug effects Ion Pumps/drug effects,physiology Molecular Sequence Data Multienzyme Complexes/drug effects,physiology Multigene Family Mutation Operon/drug effects Repressor Proteins/genetics,metabolism Trans-Activators/genetics,metabolism
Chemicals
Bacterial Proteins DNA-Binding Proteins Ion Pumps Multienzyme Complexes Repressor Proteins Trans-Activators Antimony Arsenite Transporting ATPases Arsenic Bismuth
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
López-Maury Luis
Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas, Universidad de Sevilla, E-41092 Seville, Spain.
Florencio Francisco J
Reyes José C
References (43)
43 references, click to expand
  1. Mechanism of the ArsA ATPase.
    Biochim Biophys Acta. 1999 Dec 6;1461(2):207-15 PMID: 10581357
  2. Phosphate transport and arsenate resistance in the cyanobacterium Anabaena variabilis.
    J Bacteriol. 1988 Mar;170(3):1143-7 PMID: 3125150
  3. Purification and characterization of ACR2p, the Saccharomyces cerevisiae arsenate reductase.
    J Biol Chem. 2000 Jul 14;275(28):21149-57 PMID: 10801893
  4. Structure of the ArsA ATPase: the catalytic subunit of a heavy metal resistance pump.
    EMBO J. 2000 Sep 1;19(17):4838-45 PMID: 10970874
  5. The phosphatase C(X)5R motif is required for catalytic activity of the Saccharomyces cerevisiae Acr2p arsenate reductase.
    J Biol Chem. 2001 Sep 14;276(37):34738-42 PMID: 11461905
  6. A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers.
    Gene. 1988 Aug 15;68(1):119-38 PMID: 2851487
  7. Molecular characterization of an anion pump. The ArsB protein is the membrane anchor for the ArsA protein.
    J Biol Chem. 1990 Jan 5;265(1):190-4 PMID: 1688427
  8. A promoter-probe vector-host system for the cyanobacterium, Synechocystis PCC6803.
    Gene. 1989 Dec 14;84(2):257-66 PMID: 2515116
  9. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences.
    J Bacteriol. 1990 Jun;172(6):3138-45 PMID: 2160938
  10. Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9474-8 PMID: 1409657
  11. Metalloregulated expression of the ars operon.
    J Biol Chem. 1993 Jan 5;268(1):52-8 PMID: 8416957
  12. Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria.
    Nucleic Acids Res. 1992 Dec 11;20(23):6331-7 PMID: 1282240
  13. The arsD gene encodes a second trans-acting regulatory protein of the plasmid-encoded arsenical resistance operon.
    Mol Microbiol. 1993 May;8(3):615-23 PMID: 8326869
  14. Pathways of As(III) detoxification in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5001-6 PMID: 10220408
  15. Families of arsenic transporters.
    Trends Microbiol. 1999 May;7(5):207-12 PMID: 10354596
  16. Arsenate reductase from S. aureus plasmid pI258 is a phosphatase drafted for redox duty.
    Nat Struct Biol. 2001 Oct;8(10):843-7 PMID: 11573087
  17. Insights into the structure, solvation, and mechanism of ArsC arsenate reductase, a novel arsenic detoxification enzyme.
    Structure. 2001 Nov;9(11):1071-81 PMID: 11709171
  18. Bacillus subtilis arsenate reductase is structurally and functionally similar to low molecular weight protein tyrosine phosphatases.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13577-82 PMID: 11698660
  19. A two-component signal transduction system involved in nickel sensing in the cyanobacterium Synechocystis sp. PCC 6803.
    Mol Microbiol. 2002 Jan;43(1):247-56 PMID: 11849552
  20. Public health. Worldwide occurrences of arsenic in ground water.
    Science. 2002 Jun 21;296(5576):2143-5 PMID: 12077387
  21. Public health. Arsenic epidemiology and drinking water standards.
    Science. 2002 Jun 21;296(5576):2145-6 PMID: 12077388
  22. All intermediates of the arsenate reductase mechanism, including an intramolecular dynamic disulfide cascade.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8506-11 PMID: 12072565
  23. Microbial arsenic: from geocycles to genes and enzymes.
    FEMS Microbiol Rev. 2002 Aug;26(3):311-25 PMID: 12165430
  24. Biochemistry of arsenic detoxification.
    FEBS Lett. 2002 Oct 2;529(1):86-92 PMID: 12354618
  25. Arsenate reductases in prokaryotes and eukaryotes.
    Environ Health Perspect. 2002 Oct;110 Suppl 5:745-8 PMID: 12426124
  26. The Saccharomyces cerevisiae Arr4p is involved in metal and heat tolerance.
    Biometals. 2003 Sep;16(3):369-78 PMID: 12680698
  27. Arsenic accumulation in Great Barrier Reef invertebrates.
    Science. 1981 Jan 30;211(4481):482-3 PMID: 7455685
  28. Identification of a putative metal binding site in a new family of metalloregulatory proteins.
    J Biol Chem. 1994 Aug 5;269(31):19826-9 PMID: 8051064
  29. The chromosomal arsR gene of Escherichia coli encodes a trans-acting metalloregulatory protein.
    J Biol Chem. 1996 Feb 2;271(5):2427-32 PMID: 8576202
  30. The role of arsenic-thiol interactions in metalloregulation of the ars operon.
    J Biol Chem. 1996 Apr 19;271(16):9291-7 PMID: 8621591
  31. Expression of the Escherichia coli chromosomal ars operon.
    Can J Microbiol. 1996 Jul;42(7):662-71 PMID: 8764681
  32. Virulence and arsenic resistance in Yersiniae.
    J Bacteriol. 1997 Feb;179(3):612-9 PMID: 9006011
  33. Metalloregulatory properties of the ArsD repressor.
    J Biol Chem. 1997 May 30;272(22):14257-62 PMID: 9162059
  34. Dimerization is essential for DNA binding and repression by the ArsR metalloregulatory protein of Escherichia coli.
    J Biol Chem. 1997 Jun 20;272(25):15734-8 PMID: 9188467
  35. The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport.
    J Biol Chem. 1997 Nov 28;272(48):30061-6 PMID: 9374482
  36. Nitrogen availability and electron transport control the expression of glnB gene (encoding PII protein) in the cyanobacterium Synechocystis sp. PCC 6803.
    Plant Mol Biol. 1997 Dec;35(6):723-34 PMID: 9426594
  37. The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite.
    J Bacteriol. 1998 Apr;180(7):1655-61 PMID: 9537360
  38. Biochemical characterization of the human arsenite-stimulated ATPase (hASNA-I).
    J Biol Chem. 1998 Aug 28;273(35):22173-6 PMID: 9712828
  39. An SmtB-like repressor from Synechocystis PCC 6803 regulates a zinc exporter.
    Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10728-33 PMID: 9724772
  40. Saccharomyces cerevisiae ACR2 gene encodes an arsenate reductase.
    FEMS Microbiol Lett. 1998 Nov 1;168(1):127-36 PMID: 9812373
  41. Arsenic and drinking water contamination.
    Science. 1999 Mar 5;283(5407):1458-9 PMID: 10206874
  42. Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon.
    J Biol Chem. 1986 Nov 15;261(32):15030-8 PMID: 3021763
  43. The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli.
    Appl Environ Microbiol. 2000 May;66(5):1826-33 PMID: 10788346
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2003-09-00
Pages
5363-71
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC193754
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com