Abstract
Novel nuclear magnetic resonance spectroscopy techniques, designated metabolic observation, were used to study aromatic compound degradation by the soil bacterium Acinetobacter calcoaceticus. Bacteria which had been rendered spectroscopically invisible by growth with deuterated (2H) medium were used to inoculate cultures in which natural-abundance 1H hydrogen isotopes were provided solely by aromatic carbon sources in an otherwise 2H medium. Samples taken during the incubation of these cultures were analyzed by proton nuclear magnetic resonance spectroscopy, and proton signals were correlated with the corresponding aromatic compounds or their metabolic descendants. This approach allowed the identification and quantitation of metabolites which accumulated during growth. This in vivo metabolic monitoring facilitated studies of catabolism in the presence of multiple carbon sources, a topic about which relatively little is known. A. calcoaceticus initiates aromatic compound dissimilation by forming catechol or protocatechuate from a variety of substrates. Degradation proceeds via the beta-ketoadipate pathway, comprising two discrete branches that convert catechol or protocatechuate to tricarboxylic acid cycle intermediates. As shown below, when provided with several carbon sources simultaneously, all degraded via the beta-ketoadipate pathway, A. calcoaceticus preferentially degraded specific compounds. For example, benzoate, degraded via the catechol branch, was consumed in preference to p-hydroxybenzoate, degraded via the protocatechuate branch, when both compounds were present. To determine if this preference were governed by metabolites unique to catechol degradation, pathway mutants were constructed. Studies of these mutants indicated that the product of catechol ring cleavage, cis,cis-muconate, inhibited the utilization of p-hydroxybenzoate in the presence of benzoate. The accumulation of high levels of cis,cis-muconate also appeared to be toxic to the cells.
MeSH Terms
Acinetobacter calcoaceticus/genetics,growth & development,metabolism
Adipates/metabolism
Benzoates/metabolism
Catechols/metabolism
Culture Media
Hydroxybenzoates/metabolism
Magnetic Resonance Spectroscopy
Mutation
Parabens/metabolism
Sorbic Acid/analogs & derivatives,metabolism
Chemicals
Adipates
Benzoates
Catechols
Culture Media
Hydroxybenzoates
Parabens
3-oxoadipic acid
protocatechuic acid
muconic acid
4-hydroxybenzoic acid
Sorbic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gaines G L
Isogenetics, Inc., Chicago Technology Park, Illinois 60612, USA. glgaines@merle.acns.nwu.edu.
Smith L
Neidle E L
References (25)
25 references, click to expand
-
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
Gene. 1985;33(1):103-19
PMID: 2985470
-
Transformation of Acinetobacter calco-aceticus (Bacterium anitratum).
J Bacteriol. 1969 Apr;98(1):281-8
PMID: 5781579
-
The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers.
Gene. 1982 Oct;19(3):259-68
PMID: 6295879
-
In vitro insertional mutagenesis with a selectable DNA fragment.
Gene. 1984 Sep;29(3):303-13
PMID: 6237955
-
Cloning and expression of Acinetobacter calcoaceticus catBCDE genes in Pseudomonas putida and Escherichia coli.
J Bacteriol. 1986 Feb;165(2):557-63
PMID: 3003031
-
NMR studies of a complex of deuterated calmodulin with melittin.
Proc Natl Acad Sci U S A. 1986 Jun;83(11):3634-8
PMID: 3459148
-
Applications of NMR to studies of tissue metabolism.
Annu Rev Biophys Biophys Chem. 1986;15:377-402
PMID: 3521659
-
Cloning and expression in Escherichia coli of Acinetobacter calcoaceticus genes for benzoate degradation.
J Bacteriol. 1987 Dec;169(12):5496-503
PMID: 2824437
-
High-resolution NMR studies of Saccharomyces cerevisiae.
Annu Rev Microbiol. 1987;41:595-616
PMID: 3318680
-
Characterization of Acinetobacter calcoaceticus catM, a repressor gene homologous in sequence to transcriptional activator genes.
J Bacteriol. 1989 Oct;171(10):5410-21
PMID: 2793826
-
Enzyme regulation of metabolic flux.
Methods Enzymol. 1989;177:417-34
PMID: 2607990
-
NMR studies of metabolism.
Annu Rev Biophys Biophys Chem. 1990;19:43-67
PMID: 2194483
-
NMR studies of body fluids.
NMR Biomed. 1989 Dec;2(5-6):246-56
PMID: 2701808
-
13C NMR detection of folate-mediated serine and glycine synthesis in vivo in Saccharomyces cerevisiae.
Biochemistry. 1992 Sep 22;31(37):8713-9
PMID: 1390656
-
Identification of the transcriptional activator pobR and characterization of its role in the expression of pobA, the structural gene for p-hydroxybenzoate hydroxylase in Acinetobacter calcoaceticus.
J Bacteriol. 1993 Jul;175(14):4499-506
PMID: 8331077
-
Acetate utilization is inhibited by benzoate in Alcaligenes eutrophus: evidence for transcriptional control of the expression of acoE coding for acetyl coenzyme A synthetase.
J Bacteriol. 1995 Oct;177(20):5826-33
PMID: 7592330
-
catM encodes a LysR-type transcriptional activator regulating catechol degradation in Acinetobacter calcoaceticus.
J Bacteriol. 1995 Oct;177(20):5891-8
PMID: 7592340
-
Repression of 4-hydroxybenzoate transport and degradation by benzoate: a new layer of regulatory control in the Pseudomonas putida beta-ketoadipate pathway.
J Bacteriol. 1995 Dec;177(24):7033-40
PMID: 8522507
-
The beta-ketoadipate pathway and the biology of self-identity.
Annu Rev Microbiol. 1996;50:553-90
PMID: 8905091
-
Kinetic studies of pigment synthesis by non-sulfur purple bacteria.
J Cell Physiol. 1957 Feb;49(1):25-68
PMID: 13416343
-
1H NMR spin-echo spectroscopy of human erythrocytes. Transformation of exogenous compounds.
NMR Biomed. 1990 Dec;3(6):248-58
PMID: 2092740
-
Deuterated organisms: cultivation and uses.
Science. 1966 Mar 11;151(3715):1187-94
PMID: 5325694
-
The conversion of catechol and protocatechuate to beta-ketoadipate by Pseudomonas putida.
J Biol Chem. 1966 Aug 25;241(16):3776-86
PMID: 5916391
-
Regulation of the enzymes of the beta-ketoadipate pathway in Moraxella calcoacetica. 1. General aspects.
Eur J Biochem. 1967 May;1(3):289-300
PMID: 6060184
-
Interspecies transformation of Acinetobacter: genetic evidence for a ubiquitous genus.
J Bacteriol. 1972 Nov;112(2):917-31
PMID: 4563985