Abstract
Swarming is an adaptation of many bacteria to growth on surfaces. A search for genes controlling swarmer cell differentiation of Vibrio parahaemolyticus identified a novel three-gene operon that potentially encodes a pyridoxal-phosphate-dependent enzyme, an extracellular solute-binding protein, and a membrane-bound GGDEF- and EAL-motif sensory protein. The functions of these motifs, which are named after conserved amino acid sequences, are unknown, although the domains are found singly and in combination in a variety of bacterial signaling proteins. Studies with translational fusions supported the predicted localization of the gene products. When the operon was overexpressed, swarmer cell gene transcription was induced in liquid culture. Mutants with defects in any of the three genes exhibited decreased swarming and lateral flagellar (laf) gene expression. Complementation studies confirmed an operon organization and suggested that all three genes participated in laf regulation. The lesions that decreased swarming increased capsular polysaccharide (CPS) production, and overexpression of the operon inhibited transcription of the CPS gene cpsA. Thus, the scrABC locus appears to inversely regulate two gene systems that are pertinent to colonization of surface swarming and CPS.
MeSH Terms
ATP-Binding Cassette Transporters/genetics,metabolism,physiology
Bacterial Capsules/biosynthesis
Bacterial Proteins/genetics
Carboxypeptidases/genetics
Flagella
Gene Expression Regulation, Bacterial
Genes, Reporter
Glycoside Hydrolases/genetics,metabolism,physiology
Lac Operon
Operon/physiology
Phosphoenolpyruvate Sugar Phosphotransferase System/genetics,metabolism,physiology
Transaminases/genetics,metabolism,physiology
Vibrio parahaemolyticus/genetics,physiology
beta-Fructofuranosidase
Chemicals
ATP-Binding Cassette Transporters
Bacterial Proteins
hook protein, bacterial flagellum
Transaminases
Phosphoenolpyruvate Sugar Phosphotransferase System
phosphoenolpyruvate-sucrose phosphotransferase
Glycoside Hydrolases
beta-Fructofuranosidase
Carboxypeptidases
CpsA protein, Sulfolobus solfataricus
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Boles Blaise R
Department of Microbiology, The University of Iowa, Iowa City, IA 52242, USA.
McCarter Linda L
References (23)
23 references, click to expand
-
Phosphate regulation of gene expression in Vibrio parahaemolyticus.
J Bacteriol. 1987 Aug;169(8):3441-9
PMID: 3038839
-
Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus.
J Bacteriol. 1986 Jul;167(1):210-8
PMID: 3013835
-
Genetic analysis in vibrio.
Methods Enzymol. 1991;204:515-36
PMID: 1943785
-
An application of a simple method for the preparation of bacterial DNA.
Biotechniques. 1992 Nov;13(5):696-8
PMID: 1358130
-
Identification of genes encoding components of the swarmer cell flagellar motor and propeller and a sigma factor controlling differentiation of Vibrio parahaemolyticus.
J Bacteriol. 1993 Jun;175(11):3361-71
PMID: 8501040
-
MotX, the channel component of the sodium-type flagellar motor.
J Bacteriol. 1994 Oct;176(19):5988-98
PMID: 7928960
-
Three kanamycin resistance gene cassettes with different polylinkers.
Biotechniques. 1995 Jan;18(1):52, 54, 56
PMID: 7702853
-
Periodic phenomena in Proteus mirabilis swarm colony development.
J Bacteriol. 1996 Nov;178(22):6525-38
PMID: 8932309
-
The lonS gene regulates swarmer cell differentiation of Vibrio parahaemolyticus.
J Bacteriol. 1997 Jan;179(1):107-14
PMID: 8981986
-
A simple screen for permissive sites in proteins: analysis of Escherichia coli lac permease.
J Mol Biol. 1997 Mar 28;267(2):250-63
PMID: 9096223
-
Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes.
J Bacteriol. 1998 Sep;180(17):4416-25
PMID: 9721278
-
The bspA locus of Lactobacillus fermentum BR11 encodes an L-cystine uptake system.
J Bacteriol. 1999 Apr;181(7):2192-8
PMID: 10094698
-
Surface-induced swarmer cell differentiation of Vibrio parahaemolyticus.
Mol Microbiol. 1990 Jul;4(7):1057-62
PMID: 2233248
-
Dynamic aspects of the structured cell population in a swarming colony of Proteus mirabilis.
J Bacteriol. 2000 Jan;182(2):385-93
PMID: 10629184
-
Insertional inactivation of genes encoding components of the sodium-type flagellar motor and switch of Vibrio parahaemolyticus.
J Bacteriol. 2000 Feb;182(4):1035-45
PMID: 10648530
-
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
PMID: 10829079
-
Analysis of the polar flagellar gene system of Vibrio parahaemolyticus.
J Bacteriol. 2000 Jul;182(13):3693-704
PMID: 10850984
-
The multiple identities of Vibrio parahaemolyticus.
J Mol Microbiol Biotechnol. 1999 Aug;1(1):51-7
PMID: 10941784
-
Novel domains of the prokaryotic two-component signal transduction systems.
FEMS Microbiol Lett. 2001 Sep 11;203(1):11-21
PMID: 11557134
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Induction of swarming in Vibrio parahaemolyticus.
Arch Microbiol. 1974;101(4):357-63
PMID: 4455130
-
Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants.
Gene. 1982 Jun;18(3):289-96
PMID: 6290332
-
Simple, rapid, and quantitative release of periplasmic proteins by chloroform.
J Bacteriol. 1984 Dec;160(3):1181-3
PMID: 6501229