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PMID: 9922240 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

A four-dimensional view of assembly of a morphogenetic protein during sporulation in Bacillus subtilis.

Journal of bacteriology ·Vol. 181 ·No. 3 ·1999-02-00 ·Pages 781-90

Price KD, Losick R

Abstract

We report the use of a fusion to the green fluorescent protein to visualize the assembly of the morphogenetic protein SpoIVA around the developing forespore during the process of sporulation in the bacterium Bacillus subtilis. Using a deconvolution algorithm to process digitally-collected optical sections, we show that SpoIVA, which is synthesized in the mother cell chamber of the sporangium, assembled into a spherical shell around the outer surface of the forespore. Time-lapse fluorescence microscopy showed that this assembly process commenced at the time of polar division and seemed to continue after engulfment of the forespore was complete. SpoIVA remained present throughout the late stages of morphogenesis and was present as a component of the fully mature spore. Evidence indicates that assembly of SpoIVA depended on the extreme C-terminal region of the protein and an additional region that directly or indirectly facilitated interaction among SpoIVA molecules. The N- and C-terminal regions of SpoIVA, including the extreme C terminus, are highly similar to the corresponding regions of the homologous protein from the distantly related endospore-forming bacterium Clostridium acetobutylicum, attesting to their importance in the function of the protein. Finally, we show that proper localization of SpoIVA required the expression of one or more genes which, like spoIVA, are under the control of the mother cell transcription factor sigmaE. One such gene was spoVM, whose product was required for efficient targeting of SpoIVA to the outer surface of the forespore.

MeSH Terms
Amino Acid Sequence Bacillus subtilis/cytology,genetics,physiology Bacterial Proteins/biosynthesis,chemistry,genetics Clostridium/physiology DNA-Binding Proteins/biosynthesis,chemistry Gene Expression Regulation, Bacterial Green Fluorescent Proteins Luminescent Proteins/biosynthesis,genetics Microscopy, Fluorescence Molecular Sequence Data Recombinant Fusion Proteins/analysis,biosynthesis Sequence Alignment Sequence Homology, Amino Acid Sigma Factor Spores, Bacterial/physiology Time Factors Transcription Factors
Chemicals
Bacterial Proteins DNA-Binding Proteins Luminescent Proteins Recombinant Fusion Proteins Sigma Factor Transcription Factors spoIIR protein, Bacillus subtilis spore-specific proteins, Bacillus Green Fluorescent Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Price K D
Department of Molecular and Cellular Biology, The Biological Laboratories, Harvard University, Cambridge, Massachusetts 02138, USA.
Losick R
References (45)
45 references, click to expand
  1. Characterization of bofA, a gene involved in intercompartmental regulation of pro-sigma K processing during sporulation in Bacillus subtilis.
    J Bacteriol. 1992 May;174(10):3177-84 PMID: 1577688
  2. Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis.
    J Bacteriol. 1992 Jan;174(2):575-85 PMID: 1729246
  3. Characterization of a sporulation gene, spoIVA, involved in spore coat morphogenesis in Bacillus subtilis.
    J Bacteriol. 1992 Jan;174(2):586-94 PMID: 1729247
  4. Alteration of the Bacillus subtilis glutamine synthetase results in overproduction of the enzyme.
    J Bacteriol. 1977 Sep;131(3):981-7 PMID: 19424
  5. FtsZ ring structure associated with division in Escherichia coli.
    Nature. 1991 Nov 14;354(6349):161-4 PMID: 1944597
  6. Establishment of cell type by compartmentalized activation of a transcription factor.
    Science. 1991 Oct 25;254(5031):562-5 PMID: 1948031
  7. 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
  8. A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome.
    Nucleic Acids Res. 1989 Jun 12;17(11):4410 PMID: 2500645
  9. Chromosomal rearrangement generating a composite gene for a developmental transcription factor.
    Science. 1989 Jan 27;243(4890):507-12 PMID: 2536191
  10. Genetic analysis of Bacillus subtilis spo mutations generated by Tn917-mediated insertional mutagenesis.
    Genetics. 1987 Dec;117(4):603-17 PMID: 2828153
  11. Mutants defective in bacterial chemotaxis show modified protein phosphorylation.
    Cell. 1988 Apr 8;53(1):89-96 PMID: 2832069
  12. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  13. 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
  14. 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
  15. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis.
    Cell. 1988 Apr 8;53(1):79-87 PMID: 3280143
  16. Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance.
    Biochem J. 1969 Jun;113(1):29-37 PMID: 4185146
  17. Mapping of asporogenous mutations of Bacillus subtilis: a minimum estimate of the number of sporeulation operons.
    J Bacteriol. 1973 Jun;114(3):1241-53 PMID: 4197271
  18. 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
  19. Construction of a cloning site near one end of Tn917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposon-borne erm gene.
    Plasmid. 1984 Jul;12(1):1-9 PMID: 6093169
  20. 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
  21. Use of green fluorescent protein for visualization of cell-specific gene expression and subcellular protein localization during sporulation in Bacillus subtilis.
    J Bacteriol. 1995 Oct;177(20):5906-11 PMID: 7592342
  22. Use of immunofluorescence to visualize cell-specific gene expression during sporulation in Bacillus subtilis.
    J Bacteriol. 1995 Jun;177(12):3386-93 PMID: 7768847
  23. Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis.
    J Bacteriol. 1995 Jan;177(1):166-75 PMID: 8002614
  24. Overproducing the Bacillus subtilis mother cell sigma factor precursor, Pro-sigma K, uncouples sigma K-dependent gene expression from dependence on intercompartmental communication.
    J Bacteriol. 1994 Jul;176(13):3936-43 PMID: 8021176
  25. Cloning and characterization of spoVR, a gene from Bacillus subtilis involved in spore cortex formation.
    J Bacteriol. 1994 Apr;176(7):2003-12 PMID: 8144469
  26. Guanine nucleotide-dependent assembly of FtsZ into filaments.
    J Bacteriol. 1994 May;176(9):2754-8 PMID: 8169229
  27. New improved lacZ gene fusion vectors.
    Gene. 1993 Oct 29;133(1):99-102 PMID: 8224902
  28. An unusually small gene required for sporulation by Bacillus subtilis.
    Mol Microbiol. 1993 Aug;9(4):761-71 PMID: 8231808
  29. Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis.
    Genes Dev. 1994 Jan;8(2):234-44 PMID: 8299942
  30. Green fluorescent protein as a marker for gene expression.
    Science. 1994 Feb 11;263(5148):802-5 PMID: 8303295
  31. A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus.
    Science. 1993 Feb 26;259(5099):1330-5 PMID: 8446902
  32. Polar location of the chemoreceptor complex in the Escherichia coli cell.
    Science. 1993 Mar 19;259(5102):1717-23 PMID: 8456299
  33. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):519-23 PMID: 8552673
  34. Cell cycle-controlled proteolysis of a flagellar motor protein that is asymmetrically distributed in the Caulobacter predivisional cell.
    EMBO J. 1996 May 15;15(10):2393-406 PMID: 8665847
  35. Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy.
    Mol Microbiol. 1995 Nov;18(3):459-70 PMID: 8748030
  36. Use of green fluorescent protein for detection of cell-specific gene expression and subcellular protein localization during sporulation in Bacillus subtilis.
    Microbiology. 1996 Apr;142 ( Pt 4):733-40 PMID: 8936302
  37. Molecular genetics of sporulation in Bacillus subtilis.
    Annu Rev Genet. 1996;30:297-41 PMID: 8982457
  38. Subcellular localization of proteins governing the proteolytic activation of a developmental transcription factor in Bacillus subtilis.
    Genes Cells. 1996 Jun;1(6):529-42 PMID: 9078383
  39. Protein localization and cell fate in bacteria.
    Science. 1997 May 2;276(5313):712-8 PMID: 9115191
  40. Disappearance of the sigma E transcription factor from the forespore and the SpoIIE phosphatase from the mother cell contributes to establishment of cell-specific gene expression during sporulation in Bacillus subtilis.
    J Bacteriol. 1997 May;179(10):3331-41 PMID: 9150232
  41. Regulation of the Caulobacter flagellar gene hierarchy; not just for motility.
    Mol Microbiol. 1997 Apr;24(2):233-9 PMID: 9159510
  42. SpoVM, a small protein essential to development in Bacillus subtilis, interacts with the ATP-dependent protease FtsH.
    J Bacteriol. 1997 Sep;179(17):5534-42 PMID: 9287010
  43. Bacterial cell division.
    Annu Rev Cell Dev Biol. 1997;13:395-424 PMID: 9442879
  44. A green light for the bacterial cytoskeleton.
    Trends Microbiol. 1998 Jun;6(6):233-8 PMID: 9675800
  45. Evidence for common sites of contact between the antisigma factor SpoIIAB and its partners SpoIIAA and the developmental transcription factor sigmaF in Bacillus subtilis.
    J Mol Biol. 1998 Dec 4;284(3):557-68 PMID: 9826498
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1999-02-00
Pages
781-90
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC93443
Subset
IM
Grants
NIGMS NIH HHS · GM181568 · United States
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