Abstract
Bacillus subtilis grown at 37 degrees C synthesizes saturated fatty acids with only traces of unsaturated fatty acids (UFAs). However, when cultures growing at 37 degrees C are transferred to 20 degrees C, UFA synthesis is induced. We report the identification and characterization of the gene encoding the fatty acid desaturase of B. subtilis. This gene, called des, was isolated by complementation of Escherichia coli strains with mutations in either of two different genes of UFA synthesis. The des gene encodes a polypeptide of 352 amino acid residues containing the three conserved histidine cluster motifs and two putative membrane-spanning domains characteristic of the membrane-bound desaturases of plants and cyanobacteria. Expression of the des gene in E. coli resulted in desaturation of palmitic acid moieties of the membrane phospholipids to give the novel mono-UFA cis-5-hexadecenoic acid, indicating that the B. subtilis des gene product is a delta5 acyl-lipid desaturase. The des gene was disrupted, and the resulting null mutant strains were unable to synthesize UFAs upon a shift to low growth temperatures. The des null mutant strain grew as well as its congenic parent at 20 or 37 degrees C but showed severely reduced survival during stationary phase. Analysis of operon fusions in which the des promoter directed the synthesis of a lacZ reporter gene showed that des expression is repressed at 37 degrees C, but a shift of cultures from 37 to 20 degrees C resulted in a 10- to 15-fold increase in transcription. This is the first report of a membrane phospholipid desaturase in a nonphotosynthetic organism and the first direct evidence for cold induction of a desaturase.
MeSH Terms
Amino Acid Sequence
Bacillus subtilis/enzymology,genetics,growth & development
Cell Membrane/enzymology
Cold Temperature
Conserved Sequence
DNA Primers
Escherichia coli/enzymology,genetics
Fatty Acid Desaturases/biosynthesis,genetics
Gene Expression Regulation, Bacterial
Genetic Complementation Test
Histidine
Kinetics
Polymerase Chain Reaction
Protein Conformation
Temperature
Chemicals
DNA Primers
Histidine
phospholipid desaturase
Fatty Acid Desaturases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Aguilar P S
Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Argentina.
Cronan J E
de Mendoza D
References (19)
19 references, click to expand
-
Genetic and biochemical analyses of Escherichia coli mutants altered in the temperature-dependent regulation of membrane lipid composition.
J Bacteriol. 1983 Apr;154(1):221-30
PMID: 6339472
-
Induction of proteins in response to low temperature in Escherichia coli.
J Bacteriol. 1987 May;169(5):2092-5
PMID: 3553157
-
Eight histidine residues are catalytically essential in a membrane-associated iron enzyme, stearoyl-CoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase.
Biochemistry. 1994 Nov 1;33(43):12787-94
PMID: 7947684
-
Temperature-regulated mRNA accumulation and stabilization for fatty acid desaturase genes in the cyanobacterium Synechococcus sp. strain PCC 7002.
Mol Microbiol. 1997 Mar;23(6):1281-92
PMID: 9106218
-
A simple method for displaying the hydropathic character of a protein.
J Mol Biol. 1982 May 5;157(1):105-32
PMID: 7108955
-
Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance.
Microbiol Rev. 1991 Jun;55(2):288-302
PMID: 1886522
-
Identification of a membrane protein involved in activation of the KinB pathway to sporulation in Bacillus subtilis.
J Bacteriol. 1996 Feb;178(4):1178-86
PMID: 8576055
-
Evolutionary relationships among eubacterial groups as inferred from GroEL (chaperonin) sequence comparisons.
Int J Syst Bacteriol. 1994 Jul;44(3):527-33
PMID: 7520741
-
DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis.
Mol Microbiol. 1994 Mar;11(5):933-41
PMID: 8022269
-
The complete genome sequence of the gram-positive bacterium Bacillus subtilis.
Nature. 1997 Nov 20;390(6657):249-56
PMID: 9384377
-
TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE.
Proc Natl Acad Sci U S A. 1958 Oct 15;44(10):1072-8
PMID: 16590310
-
Some like it cold: response of microorganisms to cold shock.
Arch Microbiol. 1996 Nov;166(5):293-300
PMID: 8929274
-
Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli.
Cell. 1993 Jan 29;72(2):165-8
PMID: 8425216
-
L-cysteine biosynthesis in Bacillus subtilis: identification, sequencing, and functional characterization of the gene coding for phosphoadenylylsulfate sulfotransferase.
J Bacteriol. 1997 Feb;179(3):976-81
PMID: 9006060
-
Biosynthesis of unsaturated fatty acids by bacilli. Hyperinduction and modulation of desaturase synthesis.
J Biol Chem. 1977 Jun 10;252(11):3660-70
PMID: 405386
-
The effect of temperature on the formation of delta 5-unsaturated fatty acids by bacilli.
Biochim Biophys Acta. 1967 Dec 5;144(3):701-3
PMID: 4294907
-
Regulation of the synthesis of unsaturated fatty acids by growth temperature in Bacillus subtilis.
Mol Microbiol. 1993 May;8(3):535-42
PMID: 8326865
-
The cold-shock response--a hot topic.
Mol Microbiol. 1994 Mar;11(5):811-8
PMID: 8022259
-
Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria.
Biochem J. 1995 May 15;308 ( Pt 1):1-8
PMID: 7755550