Home LiteratureArticle Details
PMID: 8419299 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Sporulation gene spoIIB from Bacillus subtilis.

Journal of bacteriology ·Vol. 175 ·No. 2 ·1993-01-00 ·Pages 528-40

Margolis PS, Driks A, Losick R

Abstract

We have cloned and characterized the sporulation gene spoIIB from Bacillus subtilis. In extension of previous nucleotide sequence analysis, our results show that the order of genes in the vicinity of spoIIB is valS folC comC spoIIB orfA orfB mreB mreC mreD minC minD spoIVFA spoIVFB L20 orfX L24 spoOB obg pheB pheA. All 20 genes have the same orientation; the direction of transcription is from valS to pheA. We show that spoIIB is a 332-codon-long open reading frame whose transcription is under sporulation control. The deduced amino acid sequence of the spoIIB gene product, a 36-kDa polypeptide, is highly charged and contains a stretch of uncharged amino acids that could correspond to a transmembrane segment. Surprisingly, mutations in spoIIB, including an in vitro-constructed null mutation, cause only a mild impairment of spore formation in certain otherwise wild-type bacteria. However, when combined with mutations in another sporulation gene, spoVG, mutations in spoIIB cause a severe block in spore formation at the stage (stage II) of septum formation. (As with spoIIB mutations, mutations in spoVG cause little impairment in sporulation on their own.) The nature of the spoIIB spoVG mutant phenotype is discussed in terms of the events involved in the maturation of the sporulation septum and in the activation of sporulation transcription factors sigma F and sigma E.

MeSH Terms
Amino Acid Sequence Bacillus subtilis/genetics,physiology,ultrastructure Bacterial Proteins/biosynthesis,genetics Base Sequence Chromosome Walking Chromosomes, Bacterial DNA, Bacterial/genetics,isolation & purification Escherichia coli/genetics Genes, Bacterial Genotype Kinetics Microscopy, Electron Molecular Sequence Data Open Reading Frames Recombinant Fusion Proteins/metabolism Restriction Mapping Sequence Deletion Sigma Factor Spores, Bacterial/genetics,ultrastructure Transcription Factors Transcription, Genetic beta-Galactosidase/genetics,metabolism
Chemicals
Bacterial Proteins DNA, Bacterial Recombinant Fusion Proteins Sigma Factor SpoIIB protein, Bacillus subtilis Transcription Factors spoIIR protein, Bacillus subtilis spore-specific proteins, Bacillus beta-Galactosidase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Margolis P S
Department of Cellular and Developmental Biology, Harvard University, Cambridge, Massachusetts 02138.
Driks A
Losick R
References (67)
67 references, click to expand
  1. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  2. Nucleotide sequence and complementation analysis of a polycistronic sporulation operon, spoVA, in Bacillus subtilis.
    J Gen Microbiol. 1985 May;131(5):1091-105 PMID: 3926949
  3. Transcriptional control of the Bacillus subtilis spoIID gene.
    J Bacteriol. 1986 Mar;165(3):771-9 PMID: 2419309
  4. Forespore-specific transcription of a gene in the signal transduction pathway that governs Pro-sigma K processing in Bacillus subtilis.
    Genes Dev. 1991 Mar;5(3):456-66 PMID: 1900494
  5. Cascades of sigma factors revisited.
    Mol Microbiol. 1990 Nov;4(11):1801-6 PMID: 2127951
  6. Control of transcription of the Bacillus subtilis spoIIIG gene, which codes for the forespore-specific transcription factor sigma G.
    J Bacteriol. 1991 May;173(9):2977-84 PMID: 1902213
  7. Genetic regulation of morphogenesis in Bacillus subtilis: roles of sigma E and sigma F in prespore engulfment.
    J Bacteriol. 1991 May;173(10):3159-69 PMID: 1902463
  8. Genetic evidence for interaction of sigma A with two promoters in Bacillus subtilis.
    J Bacteriol. 1991 Jun;173(11):3282-90 PMID: 1904429
  9. Sporulation operon spoIVF and the characterization of mutations that uncouple mother-cell from forespore gene expression in Bacillus subtilis.
    J Mol Biol. 1991 Oct 20;221(4):1237-56 PMID: 1942049
  10. Compartmentalized expression of a gene under the control of sporulation transcription factor sigma E in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):9934-8 PMID: 1946462
  11. Establishment of cell type by compartmentalized activation of a transcription factor.
    Science. 1991 Oct 25;254(5031):562-5 PMID: 1948031
  12. Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis.
    J Bacteriol. 1992 Jan;174(2):575-85 PMID: 1729246
  13. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis.
    Nature. 1992 Feb 13;355(6361):601-4 PMID: 1538747
  14. spoVG sequence of Bacillus megaterium and Bacillus subtilis.
    Biochim Biophys Acta. 1992 Mar 24;1130(2):229-31 PMID: 1373326
  15. Bacillus subtilis early sporulation genes kinA, spo0F, and spo0A are transcribed by the RNA polymerase containing sigma H.
    J Bacteriol. 1992 May;174(9):2771-8 PMID: 1569009
  16. Establishment of cell-specific transcription during sporulation in Bacillus subtilis.
    Mol Microbiol. 1992 Mar;6(6):689-95 PMID: 1573998
  17. Genetic structure, isolation and characterization of a Bacillus licheniformis cell wall hydrolase.
    Mol Gen Genet. 1992 Jul;234(1):129-37 PMID: 1495475
  18. Molecular cloning of the gene encoding the valyl-tRNA synthetase from Bacillus stearothermophilus.
    Gene. 1986;44(1):139-42 PMID: 3770480
  19. The effect of spo0 mutations on the expression of spo0A- and spo0F-lacZ fusions.
    Mol Gen Genet. 1986 Oct;205(1):28-33 PMID: 3099127
  20. Genetics of endospore formation in Bacillus subtilis.
    Annu Rev Genet. 1986;20:625-69 PMID: 3101583
  21. Sporulation-specific sigma factor sigma 29 of Bacillus subtilis is synthesized from a precursor protein, P31.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1784-8 PMID: 3104904
  22. Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis.
    J Bacteriol. 1987 May;169(5):2223-30 PMID: 2437099
  23. Isolation and characterization of Tn917lac-generated competence mutants of Bacillus subtilis.
    J Bacteriol. 1987 Jul;169(7):3104-9 PMID: 3036770
  24. Organization and regulation of an operon that encodes a sporulation-essential sigma factor in Bacillus subtilis.
    J Bacteriol. 1987 Jul;169(7):3329-39 PMID: 2439490
  25. The valyl-tRNA synthetase from Bacillus stearothermophilus has considerable sequence homology with the isoleucyl-tRNA synthetase from Escherichia coli.
    Biochemistry. 1987 May 5;26(9):2480-6 PMID: 3300774
  26. Primary structure of the Escherichia coli folC gene and its folylpolyglutamate synthetase-dihydrofolate synthetase product and regulation of expression by an upstream gene.
    J Biol Chem. 1987 Sep 5;262(25):12337-43 PMID: 3040739
  27. A general method for fusion of the Escherichia coli lacZ gene to chromosomal genes in Bacillus subtilis.
    J Gen Microbiol. 1986 Nov;132(11):2953-66 PMID: 3114418
  28. Use of a lacZ gene fusion to determine the dependence pattern of sporulation operon spoIIA in spo mutants of Bacillus subtilis.
    J Gen Microbiol. 1986 Nov;132(11):2967-76 PMID: 3114419
  29. Genes encoding spore coat polypeptides from Bacillus subtilis.
    J Mol Biol. 1987 Jul 5;196(1):1-10 PMID: 2821284
  30. Nucleotide sequence of Escherichia coli valyl-tRNA synthetase gene valS.
    Nucleic Acids Res. 1987 Nov 11;15(21):9081-2 PMID: 3317277
  31. Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore.
    Genes Dev. 1988 Aug;2(8):1047-54 PMID: 3139490
  32. Small, acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function, and degradation.
    Annu Rev Microbiol. 1988;42:319-38 PMID: 3059997
  33. The Bacillus subtilis spo0B stage 0 sporulation operon encodes an essential GTP-binding protein.
    J Bacteriol. 1989 Mar;171(3):1362-71 PMID: 2537815
  34. Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis.
    J Bacteriol. 1989 Aug;171(8):4121-9 PMID: 2502532
  35. Molecular cloning and characterization of comC, a late competence gene of Bacillus subtilis.
    J Bacteriol. 1989 Nov;171(11):6043-51 PMID: 2553669
  36. Cloning and expression of the gene encoding Lactobacillus casei folylpoly-gamma-glutamate synthetase in Escherichia coli and determination of its primary structure.
    J Biol Chem. 1990 Feb 15;265(5):2492-9 PMID: 2105929
  37. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene.
    Proc Natl Acad Sci U S A. 1990 Mar;87(5):1801-5 PMID: 2106683
  38. A forespore checkpoint for mother cell gene expression during development in B. subtilis.
    Cell. 1990 Jul 27;62(2):239-50 PMID: 2115401
  39. Orientation of genes in the Bacillus subtilis chromosome.
    Genetics. 1990 Aug;125(4):703-8 PMID: 2118869
  40. Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1990 Dec;87(23):9221-5 PMID: 2123551
  41. Processing of the mother-cell sigma factor, sigma K, may depend on events occurring in the forespore during Bacillus subtilis development.
    Proc Natl Acad Sci U S A. 1990 Dec;87(24):9722-6 PMID: 2124700
  42. Molecular cloning and sequencing of the upstream region of the major Bacillus subtilis autolysin gene: a modifier protein exhibiting sequence homology to the major autolysin and the spoIID product.
    J Gen Microbiol. 1992 Jun;138(6):1067-76 PMID: 1356138
  43. Identification of Bacillus subtilis genes for septum placement and shape determination.
    J Bacteriol. 1992 Nov;174(21):6717-28 PMID: 1400224
  44. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants.
    J Bacteriol. 1992 Nov;174(21):6729-42 PMID: 1400225
  45. Septal membrane fusion--a pivotal event in bacterial spore formation?
    Mol Microbiol. 1992 Sep;6(18):2565-71 PMID: 1447970
  46. Fate of transforming DNA following uptake by competent Bacillus subtilis. I. Formation and properties of the donor-recipient complex.
    J Mol Biol. 1971 Mar 14;56(2):209-21 PMID: 4994568
  47. Sporulation in Bacillus subtilis. Genetic analysis of oligosporogenous mutants.
    J Gen Microbiol. 1972 Jun;71(1):17-27 PMID: 4625070
  48. Sporulation in Bacillus subtilis. Characterization of oligosporogenous mutants and comparison of their phenotypes with those of asporogenous mutants.
    J Gen Microbiol. 1972 Jun;71(1):1-15 PMID: 4625072
  49. Regulation of expression of genes coding for small, acid-soluble proteins of Bacillus subtilis spores: studies using lacZ gene fusions.
    J Bacteriol. 1988 Jan;170(1):239-44 PMID: 3121585
  50. Genetic analysis of Bacillus subtilis spo mutations generated by Tn917-mediated insertional mutagenesis.
    Genetics. 1987 Dec;117(4):603-17 PMID: 2828153
  51. The Bacillus subtilis spoIIG operon encodes both sigma E and a gene necessary for sigma E activation.
    J Bacteriol. 1988 Feb;170(2):507-11 PMID: 2448286
  52. Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression.
    Cell. 1988 Mar 11;52(5):697-704 PMID: 3125985
  53. Characterization of the promoter region of the Bacillus subtilis spoIIE operon.
    J Bacteriol. 1988 Apr;170(4):1598-609 PMID: 2832371
  54. The GenBank genetic sequence data bank.
    Nucleic Acids Res. 1988 Mar 11;16(5):1861-3 PMID: 3353225
  55. When polymerases collide: replication and the transcriptional organization of the E. coli chromosome.
    Cell. 1988 Jun 3;53(5):679-86 PMID: 3286014
  56. Identification of the promoter for a spore coat protein gene in Bacillus subtilis and studies on the regulation of its induction at a late stage of sporulation.
    J Mol Biol. 1988 Apr 5;200(3):461-73 PMID: 3135411
  57. Deoxyribonucleic acid-binding proteins in vegetative Bacillus subtilis: alterations caused by stage O sporulation mutations.
    J Bacteriol. 1975 Nov;124(2):977-84 PMID: 810485
  58. Genetic aspects of bacterial endospore formation.
    Bacteriol Rev. 1976 Dec;40(4):908-62 PMID: 12736
  59. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  60. Novel RNA polymerase sigma factor from Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7000-4 PMID: 6784117
  61. Identification of a new developmental locus in Bacillus subtilis by construction of a deletion mutation in a cloned gene under sporulation control.
    J Bacteriol. 1981 Oct;148(1):341-51 PMID: 6793556
  62. Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis.
    Mol Gen Genet. 1982;186(3):339-46 PMID: 6181373
  63. Use of a lacZ fusion to study the role of the spoO genes of Bacillus subtilis in developmental regulation.
    Cell. 1983 Nov;35(1):275-83 PMID: 6414720
  64. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  65. Identification of a new sporulation locus, spoIIIF, in Bacillus subtilis.
    J Gen Microbiol. 1984 May;130(5):1253-61 PMID: 6432947
  66. A novel method for the rapid cloning in Escherichia coli of Bacillus subtilis chromosomal DNA adjacent to Tn917 insertions.
    Mol Gen Genet. 1984;195(3):424-33 PMID: 6088944
  67. Sequence analysis of the spo0B locus reveals a polycistronic transcription unit.
    J Bacteriol. 1985 Feb;161(2):556-62 PMID: 3918016
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1993-01-00
Pages
528-40
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC196168
Subset
IM
Grants
NIGMS NIH HHS · GM18568 · United States
Databases
GENBANK
L04519, L04520, L30805, M30805, M96343
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