Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Oct;175(19):6203–6211. doi: 10.1128/jb.175.19.6203-6211.1993

Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfpo and Escherichia coli entD genes.

T H Grossman 1, M Tuckman 1, S Ellestad 1, M S Osburne 1
PMCID: PMC206715  PMID: 8407792

Abstract

In response to iron deprivation, Bacillus subtilis secretes a catecholic siderophore, 2,3-dihydroxybenzoyl glycine, which is similar to the precursor of the Escherichia coli siderophore enterobactin. We isolated two sets of B. subtilis DNA sequences that complemented the mutations of several E. coli siderophore-deficient (ent) mutants with defective enterobactin biosynthesis enzymes. One set contained DNA sequences that complemented only an entD mutation. The second set contained DNA sequences that complemented various combinations of entB, entE, entC, and entA mutations. The two sets of DNA sequences did not appear to overlap. AB. subtilis mutant containing an insertion in the region of the entD homolog grew much more poorly in low-iron medium and with markedly different kinetics. These data indicate that (i) at least five of the siderophore biosynthesis genes of B. subtilis can function in E. coli, (ii) the genetic organization of these siderophore genes in B. subtilis is similar to that in E. coli, and (iii) the B. subtilis entD homolog is required for efficient growth in low-iron medium. The nucleotide sequence of the B. subtilis DNA contained in plasmid pENTA22, a clone expressing the B. subtilis entD homolog, revealed the presence of at least two genes. One gene was identified as sfpo, a previously reported gene involved in the production of surfactin in B. subtilis and which is highly homologous to the E. coli entD gene. We present evidence that the E. coli entD and B. subtilis sfpo genes are interchangeable and that their products are members of a new family of proteins which function in the secretion of peptide molecules.

Full text

PDF
6203

Images in this article

6210Image
on p.6210

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ames G. F., Mimura C. S., Shyamala V. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: Traffic ATPases. FEMS Microbiol Rev. 1990 Aug;6(4):429–446. doi: 10.1111/j.1574-6968.1990.tb04110.x. [DOI] [PubMed] [Google Scholar]
  2. Armstrong S. K., Pettis G. S., Forrester L. J., McIntosh M. A. The Escherichia coli enterobactin biosynthesis gene, entD: nucleotide sequence and membrane localization of its protein product. Mol Microbiol. 1989 Jun;3(6):757–766. doi: 10.1111/j.1365-2958.1989.tb00224.x. [DOI] [PubMed] [Google Scholar]
  3. Fleming T. P., Nahlik M. S., Neilands J. B., McIntosh M. A. Physical and genetic characterization of cloned enterobactin genomic sequences from Escherichia coli K-12. Gene. 1985;34(1):47–54. doi: 10.1016/0378-1119(85)90293-8. [DOI] [PubMed] [Google Scholar]
  4. Krätzschmar J., Krause M., Marahiel M. A. Gramicidin S biosynthesis operon containing the structural genes grsA and grsB has an open reading frame encoding a protein homologous to fatty acid thioesterases. J Bacteriol. 1989 Oct;171(10):5422–5429. doi: 10.1128/jb.171.10.5422-5429.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Love P. E., Lyle M. J., Yasbin R. E. DNA-damage-inducible (din) loci are transcriptionally activated in competent Bacillus subtilis. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6201–6205. doi: 10.1073/pnas.82.18.6201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Love P. E., Yasbin R. E. Genetic characterization of the inducible SOS-like system of Bacillus subtilis. J Bacteriol. 1984 Dec;160(3):910–920. doi: 10.1128/jb.160.3.910-920.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Nahlik M. S., Brickman T. J., Ozenberger B. A., McIntosh M. A. Nucleotide sequence and transcriptional organization of the Escherichia coli enterobactin biosynthesis cistrons entB and entA. J Bacteriol. 1989 Feb;171(2):784–790. doi: 10.1128/jb.171.2.784-790.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Nakano M. M., Corbell N., Besson J., Zuber P. Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis. Mol Gen Genet. 1992 Mar;232(2):313–321. doi: 10.1007/BF00280011. [DOI] [PubMed] [Google Scholar]
  9. Nakano M. M., Zuber P. Molecular biology of antibiotic production in Bacillus. Crit Rev Biotechnol. 1990;10(3):223–240. doi: 10.3109/07388559009038209. [DOI] [PubMed] [Google Scholar]
  10. Osburne M. S., Zavodny S. M., Peterson G. A. Drug-induced relaxation of supercoiled plasmid DNA in Bacillus subtilis and induction of the SOS response. J Bacteriol. 1988 Jan;170(1):442–445. doi: 10.1128/jb.170.1.442-445.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ozenberger B. A., Brickman T. J., McIntosh M. A. Nucleotide sequence of Escherichia coli isochorismate synthetase gene entC and evolutionary relationship of isochorismate synthetase and other chorismate-utilizing enzymes. J Bacteriol. 1989 Feb;171(2):775–783. doi: 10.1128/jb.171.2.775-783.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Payne S. M. Iron and virulence in the family Enterobacteriaceae. Crit Rev Microbiol. 1988;16(2):81–111. doi: 10.3109/10408418809104468. [DOI] [PubMed] [Google Scholar]
  13. Schwyn B., Neilands J. B. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987 Jan;160(1):47–56. doi: 10.1016/0003-2697(87)90612-9. [DOI] [PubMed] [Google Scholar]
  14. Sonenshein A. L., Cami B., Brevet J., Cote R. Isolation and characterization of rifampin-resistant and streptolydigin-resistant mutants of Bacillus subtilis with altered sporulation properties. J Bacteriol. 1974 Oct;120(1):253–265. doi: 10.1128/jb.120.1.253-265.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Staab J. F., Earhart C. F. EntG activity of Escherichia coli enterobactin synthetase. J Bacteriol. 1990 Nov;172(11):6403–6410. doi: 10.1128/jb.172.11.6403-6410.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. TAKAHASHI I. Transducing phages for Bacillus subtilis. J Gen Microbiol. 1963 May;31:211–217. doi: 10.1099/00221287-31-2-211. [DOI] [PubMed] [Google Scholar]
  17. Tuckman M., Osburne M. S. In vivo inhibition of TonB-dependent processes by a TonB box consensus pentapeptide. J Bacteriol. 1992 Jan;174(1):320–323. doi: 10.1128/jb.174.1.320-323.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Vandeyar M. A., Zahler S. A. Chromosomal insertions of Tn917 in Bacillus subtilis. J Bacteriol. 1986 Aug;167(2):530–534. doi: 10.1128/jb.167.2.530-534.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Way J. C., Davis M. A., Morisato D., Roberts D. E., Kleckner N. New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene. 1984 Dec;32(3):369–379. doi: 10.1016/0378-1119(84)90012-x. [DOI] [PubMed] [Google Scholar]
  21. de Lorenzo V., Wee S., Herrero M., Neilands J. B. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol. 1987 Jun;169(6):2624–2630. doi: 10.1128/jb.169.6.2624-2630.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES