Abstract
Attachment to surfaces by the prosthecate bacterium Caulobacter crescentus is mediated by an adhesive organelle, the holdfast, found at the tip of the stalk. Indirect evidence suggested that the holdfast first appears at the swarmer pole of the predivisional cell. We used fluorescently labeled lectin and transmission electron microscopy to detect the holdfast in different cell types. While the holdfast was readily detectable in stalked cells and at the stalked poles of predivisional cells, we were unable to detect the holdfast in swarmer cells or at the flagellated poles of predivisional cells. This suggests that exposure of the holdfast to the outside of the cell occurs during the differentiation of swarmer to stalked cells. To investigate the timing of holdfast synthesis and exposure to the outside of the cell, we have examined the regulation of a holdfast attachment gene, hfaA. The hfaA gene is part of a cluster of four genes (hfaABDC), identified in strain CB2A and involved in attachment of the holdfast to the polar region of the cell. We have identified the hfaA gene in the synchronizable C. crescentus strain CB15. The sequence of the CB2A hfaA promoter suggested that it was regulated by sigma54. We show that the transcription of hfaA from either strain is not dependent on sigma54. Using a hfaA-lacZ fusion, we show that the transcription of hfaA is temporally regulated during the cell cycle, with maximal expression in late-predivisional cells. This increase in expression is largely due to the preferential transcription of hfaA in the swarmer pole of the predivisional cell.
MeSH Terms
Adhesins, Bacterial/biosynthesis,genetics
Bacterial Adhesion/genetics
Caulobacter crescentus/genetics,growth & development,ultrastructure
Cell Compartmentation
Cell Cycle
Cloning, Molecular
DNA-Binding Proteins
DNA-Directed RNA Polymerases/metabolism
Gene Expression Regulation, Bacterial
Genes, Bacterial
Molecular Sequence Data
RNA Polymerase Sigma 54
Sequence Analysis, DNA
Sigma Factor/metabolism
Transcription, Genetic
Chemicals
Adhesins, Bacterial
DNA-Binding Proteins
HfaA protein, Caulobacter crescentus
Sigma Factor
DNA-Directed RNA Polymerases
RNA Polymerase Sigma 54
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Janakiraman R S
Department of Biology, Indiana University, Bloomington, Indiana 47405-6801, USA.
Brun Y V
References (30)
30 references, click to expand
-
A developmentally regulated Caulobacter flagellar promoter is activated by 3' enhancer and IHF binding elements.
Mol Biol Cell. 1992 Aug;3(8):913-26
PMID: 1392079
-
BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP.
Bacteriol Rev. 1964 Sep;28:231-95
PMID: 14220656
-
A temporally controlled sigma-factor is required for polar morphogenesis and normal cell division in Caulobacter.
Genes Dev. 1992 Dec;6(12A):2395-408
PMID: 1459461
-
The phylogeny of marine and freshwater caulobacters reflects their habitat.
J Bacteriol. 1992 Apr;174(7):2193-8
PMID: 1551840
-
Characterization of the adhesive holdfast of marine and freshwater caulobacters.
Appl Environ Microbiol. 1988 Aug;54(8):2078-85
PMID: 16347718
-
Spatial and Temporal Deposition of Adhesive Extracellular Polysaccharide Capsule and Fimbriae by Hyphomonas Strain MHS-3.
Appl Environ Microbiol. 1998 Apr;64(4):1246-55
PMID: 16349537
-
Specific binding of the transcription factor sigma-54 to promoter DNA.
Nature. 1992 Jul 30;358(6385):422-4
PMID: 1641025
-
Genetic analysis of a temporally transcribed chemotaxis gene cluster in Caulobacter crescentus.
Genetics. 1991 Oct;129(2):333-41
PMID: 1660425
-
Analysis of a Caulobacter crescentus gene cluster involved in attachment of the holdfast to the cell.
J Bacteriol. 1992 Feb;174(3):687-94
PMID: 1732204
-
Expression of positional information during cell differentiation of Caulobacter.
Cell. 1991 Jan 25;64(2):381-91
PMID: 1988153
-
Identification of genes affecting production of the adhesion organelle of Caulobacter crescentus CB2.
J Bacteriol. 1990 Sep;172(9):5425-31
PMID: 2168382
-
pBluescript II: gene mapping vectors.
Nucleic Acids Res. 1989 Nov 25;17(22):9494
PMID: 2555794
-
Use of pulsed field gel electrophoresis and transposon mutagenesis to estimate the minimal number of genes required for motility in Caulobacter crescentus.
Genetics. 1989 Dec;123(4):649-54
PMID: 2558955
-
DNA sequencing with chain-terminating inhibitors.
Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7
PMID: 271968
-
Localizing the subunit pool for the temporally regulated polar pili of Caulobacter crescentus.
J Cell Biol. 1987 Oct;105(4):1821-8
PMID: 2889742
-
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
Gene. 1985;33(1):103-19
PMID: 2985470
-
Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells.
J Bacteriol. 1977 Oct;132(1):294-301
PMID: 334726
-
Isolation of spontaneously derived mutants of Caulobacter crescentus.
Genetics. 1977 May;86(1):25-32
PMID: 407126
-
Role of transcription in the temporal control of development in Caulobacter crescentus (stalk-rifampin-RNA synthesis-DNA synthesis-motility).
Proc Natl Acad Sci U S A. 1972 Feb;69(2):447-51
PMID: 4501124
-
The pIC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation.
Gene. 1984 Dec;32(3):481-5
PMID: 6099327
-
Cloning of the major protein of the Caulobacter crescentus periodic surface layer: detection and characterization of the cloned peptide by protein expression assays.
J Bacteriol. 1984 Dec;160(3):1137-45
PMID: 6209263
-
A comprehensive set of sequence analysis programs for the VAX.
Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95
PMID: 6546423
-
The caulobacters: ubiquitous unusual bacteria.
Microbiol Rev. 1981 Mar;45(1):123-79
PMID: 7012570
-
In a class of its own--the RNA polymerase sigma factor sigma 54 (sigma N).
Mol Microbiol. 1993 Dec;10(5):903-9
PMID: 7934866
-
The expression of asymmetry during Caulobacter cell differentiation.
Annu Rev Biochem. 1994;63:419-50
PMID: 7979244
-
Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition.
Cell. 1993 Jun 4;73(5):887-901
PMID: 8098994
-
The Caulobacter crescentus holdfast: identification of holdfast attachment complex genes.
FEMS Microbiol Lett. 1994 Feb 15;116(2):175-82
PMID: 8150261
-
Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter.
Genes Dev. 1993 Oct;7(10):1979-92
PMID: 8406002
-
Transcriptional and mutational analyses of the rpoN operon in Caulobacter crescentus.
J Bacteriol. 1997 Aug;179(16):5138-47
PMID: 9260957
-
In vivo genomic footprinting analysis reveals that the complex Bradyrhizobium japonicum fixRnifA promoter region is differently occupied by two distinct RNA polymerase holoenzymes.
Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1014-9
PMID: 9448277