Plasmid-Mediated Histamine Biosynthesis in the Bacterial Fish PathogenVibrio anguillarum

doi:10.1006/plas.1998.1345

Plasmid

Volume 39, Issue 3, May 1998, Pages 235-244

Communicated by S. A. Khan

https://doi.org/10.1006/plas.1998.1345 Get rights and content

Abstract

Histamine production in bacteria-contaminated fish is the result of the presence of bacterial histidine decarboxylase activity, which converts histidine present in muscle proteins to histamine. The fish pathogenVibrio anguillarumharbors a plasmid-encoded histidine decarboxylase gene (angH) that is essential for biosynthesis of the siderophore anguibactin. However, the role ofangHin histamine biosynthesis by this pathogen has not been fully determined. Thus, the objectives of this study were to monitor the production and release of histamine by the wild-type as well as by a plasmidless strain andangHisogenic mutants generated by allelic exchange. Reverse transcription polymerase chain reaction showed that only the wild-type strain expressedangH,while noangHmessage was detected in the mutants and the plasmidless derivative. The iron uptake-deficient phenotype of one of theangHmutants confirmed the location of the mutation and the unique role of this gene in iron acquisition. Thin-layer chromatography, gas chromatography, and mass spectrometry showed that histamine was released by the strain harboring a wild-typeangHgene when grown in excess histidine. This biogenic amine was not detected in the culture supernatants of the plasmidless derivative and theangHmutant when cultured under the same experimental conditions. These results indicate thatangHis essential for histamine biosynthesis inV. anguillarum,a compound responsible for food poisoning and potentially involved in bacterial virulence. Thin-layer chromatography of wild-type culture supernatants and β-galactosidase assays using the isogenicangHmutant demonstrated that the expression of this gene is independent of the histidine concentration of the medium under both iron-rich and iron-limiting conditions.

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Citation Excerpt :
The inhibition of the decarboxylase in S. putrefaciens lead to the production of unnatural siderophores [16]. The ODC of B. pertussis is not part of the alcaligin gene cluster alcABCD [10] and shows parallels to the histidine decarboxylase from Vibrio anguillarum, which is involved in the biosynthesis of anguibactin, but only a partial protein sequence of this ODC is available [17–19]. Another decarboxylase gene (pvsE) was found to be involved in the biosynthesis of vibrioferrin in Vibrio parahaemolytics.
Lysine is a precursor for desferrioxamine siderophore biosynthesis. The pathway is often initiated by lysine decarboxylases. However, little is known about those enzymes from Actinobacteria which represents a diverse class of desferrioxamine producers. In this study we focused on the genes grdesA form Gordonia rubripertincta CWB2 and psdesA from Pimelobacter simplex VkMAC-2033D that encode decarboxylases presumed to be involved in the synthesis of desferrioxamine siderophores. The corresponding proteins GrDesA and PsDesA, were heterologously produced in Escherichia coli and purified. PsDesA was isolated bound to the cofactor pyridoxal 5-phosphate and GrDesA was purified in its apo form. PsDesA showed a moderate substrate preference for lysine (K_m = 0.17 mM, k_cat = 0.26 s⁻¹) compared to ornithine (K_m = 0.13 mM, k_cat = 0.14 s⁻¹), while GrDesA exhibited specificity for lysine (K_m = 0.13 mM, k_cat = 1.2 s⁻¹) compared to ornithine (K_m = 2.9 mM, k_cat = 0.18 s⁻¹). The maximum decarboxylase activity of PsDesA was achieved at pH 7.5 at 35 °C, although PsDesA was stable up to 40°, its relative activity decreased significantly at 50 °C. The temperature optimum (40 °C) and thermostability of GrDesA were likewise, but it exhibited maximum activity at pH range 8.0–8.5, and sharply decreased outside of this range. The expression and characterization of these two decarboxylases provides insight into the biosynthetic pathway of desferrioxamines from G. rubripertincta and P. simplex and supports the functional annotation of related pathways.
Thin-layer chromatography for the identification and semi-quantification of biogenic amines produced by bacteria
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The screening TLC method described enables the simultaneous identification and semi-quantification of eight biogenic amines with a large number of samples handled in a short period of time. The dansylation process time was drastically reduced from 80 to 18 min by increasing the reaction temperature to 100 °C. Bacteria could be classified as no, low, moderate or powerful amine producers when no spots were noticeable in TLC plates, less than 50 mg/L, from 50 to 500 mg/L, or more than 500 mg/L of amines were present in the decarboxylase broth medium, respectively. This TLC method is a simpler, faster and less expensive alternative to other methods, such as differential culture media, HPLC and even more sensitive than other TLC procedures.
Analysis of pVU3695, a plasmid encoding glutathione-dependent formaldehyde dehydrogenase activity and formaldehyde resistance in the Escherichia coli VU3695 clinical strain
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The formaldehyde resistance of Escherichia coli VU3695 is due to the expression of glutathione-dependent formaldehyde dehydrogenase (GSH-FDH) activity, which is encoded by the adhC gene located on the plasmid pVU3695. Conjugation of this plasmid to an unrelated PolA deficient strain of E. coli indicated that it encodes its own replication initiation protein and does not confer resistance to several other antimicrobial agents tested in this work. In addition, pVU3695 has homology with replicons that belong to the IncL/M plasmid incompatibility group, which are widely distributed among the Enterobacteriaceae. Curing of pVU3695 abolished the expression of formaldehyde resistance and the presence of a 46-kDa periplasmic protein immunologically related to GSH-FDH. However, the curing of pVU3695 reduced drastically but did not abolish the expression of a protein with similar electrophoretic motility, which was associated with the expression of GSH-FDH activity still present in the cytoplasm of the plasmidless derivative. The data demonstrate that E. coli VU3695 contains a chromosomal and a plasmid copy of adhC actively expressed, with the latter being involved in resistance to exogenous formaldehyde.
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Histamine (or scombroid) fish poisoning (HFP) is reviewed in a risk-assessment framework in an attempt to arrive at an informed characterisation of risk. Histamine is the main toxin involved in HFP, but the disease is not uncomplicated histamine poisoning. Although it is generally associated with high levels of histamine (≥50 mg/100 g) in bacterially contaminated fish of particular species, the pathogenesis of HFP has not been clearly elucidated. Various hypotheses have been put forward to explain why histamine consumed in spoiled fish is more toxic than pure histamine taken orally, but none has proved totally satisfactory. Urocanic acid, like histamine, an imidazole compound derived from histidine in spoiling fish, may be the “missing factor” in HFP. cis-Urocanic acid has recently been recognised as a mast cell degranulator, and endogenous histamine from mast cell degranulation may augment the exogenous histamine consumed in spoiled fish. HFP is a mild disease, but is important in relation to food safety and international trade. Consumers are becoming more demanding, and litigation following food poisoning incidents is becoming more common. Producers, distributors and restaurants are increasingly held liable for the quality of the products they handle and sell. Many countries have set guidelines for maximum permitted levels of histamine in fish. However, histamine concentrations within a spoiled fish are extremely variable, as is the threshold toxic dose. Until the identity, levels and potency of possible potentiators and/or mast-cell-degranulating factors are elucidated, it is difficult to establish regulatory limits for histamine in foods on the basis of potential health hazard. Histidine decarboxylating bacteria produce histamine from free histidine in spoiling fish. Although some are present in the normal microbial flora of live fish, most seem to be derived from post-catching contamination on board fishing vessels, at the processing plant or in the distribution system, or in restaurants or homes. The key to keeping bacterial numbers and histamine levels low is the rapid cooling of fish after catching and the maintenance of adequate refrigeration during handling and storage. Despite the huge expansion in trade in recent years, great progress has been made in ensuring the quality and safety of fish products. This is largely the result of the introduction of international standards of food hygiene and the application of risk analysis and hazard analysis and critical control point (HACCP) principles.
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^☆: J. Drozd

¹: To whom correspondence should be addressed. Fax: (513) 529–2431. E-mail:[email protected].

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Regular ArticlePlasmid-Mediated Histamine Biosynthesis in the Bacterial Fish PathogenVibrio anguillarum☆

Abstract

Anal. Biochem.

J. Microbiol. Methods

Anal. Biochem.

Plasmid

J. Biol. Chem.

J. Biol. Chem.

J. Chromatogr.

J. Biol. Chem.

J. Biol. Chem.

Anal. Biochem.

Characterization of anguibactin, a novel siderophore fromVibrio anguillarum

J. Bacteriol.

Bacterial production of histamine in some tropical fish

Microbios

A plasmid associated with virulence in the marine fish pathogenVibrio anguillarum

Nature (London)

Curing of a plasmid is correlated with an attenuation of virulence in the marine fish pathogenVibrio anguillarum.

Infect. Immun.

Chemical derivatization in gas chromatography

Journal of Chromatography Library

Purification and properties of pyridoxal-5′-phosphate-dependent histidine decarboxylases fromKlebsiella planticolaEnterobacter aerogenes.

J. Bacteriol.

Cloning, characterization, and nucleotide sequence analysis ofZymomonas mobilis

J. Bacteriol.

Regular Article
Plasmid-Mediated Histamine Biosynthesis in the Bacterial Fish PathogenVibrio anguillarum☆