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Applied and Environmental Microbiology, July 2004, p. 4293-4302, Vol. 70, No. 7
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.7.4293-4302.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Presence of Acylated Homoserine Lactones (AHLs) and AHL-Producing Bacteria in Meat and Potential Role of AHL in Spoilage of Meat

Jesper Bartholin Bruhn,1* Allan Beck Christensen,2 Lars Ravn Flodgaard,1 Kristian Fog Nielsen,3 Thomas Ostenfeld Larsen,3 Michael Givskov,2 and Lone Gram1

Centre for Biomedical Microbiology, Section of Molecular Microbiology,2 Center for Process Biotechnology, BioCentrum-DTUTechnical University of Denmark,3 Department of Seafood Research, Danish Institute for Fisheries Research DK-2800 Kgs. Lyngby, Denmark1

Received 26 September 2003/ Accepted 8 March 2004

Quorum-sensing (QS) signals (N-acyl homoserine lactones [AHLs]) were extracted and detected from five commercially produced vacuum-packed meat samples. Ninety-six AHL-producing bacteria were isolated, and 92 were identified as Enterobacteriaceae. Hafnia alvei was the most commonly identified AHL-producing bacterium. Thin-layer chromatographic profiles of supernatants from six H. alvei isolates and of extracts from spoiling meat revealed that the major AHL species had an Rf value and shape similar to N-3-oxo-hexanoyl homoserine lactone (OHHL). Liquid chromatography-mass spectrometry (MS) (high-resolution MS) analysis confirmed the presence of OHHL in pure cultures of H. alvei. Vacuum-packed meat spoiled at the same rate when inoculated with the H. alvei wild type compared to a corresponding AHL-lacking mutant. Addition of specific QS inhibitors to the AHL-producing H. alvei inoculated in meat or to naturally contaminated meat did not influence the spoilage of vacuum-packed meat. An extracellular protein of approximately 20 kDa produced by the H. alvei wild-type was not produced by the AHL-negative mutant but was restored in the mutant when complemented by OHHL, thus indicating that AHLs do have a regulatory role in H. alvei. Coinoculation of H. alvei wild-type with an AHL-deficient Serratia proteamaculans B5a, in which protease secretion is QS regulated, caused spoilage of liquid milk. By contrast, coinoculation of AHL-negative strains of H. alvei and S. proteamaculans B5a did not cause spoilage. In conclusion, AHL and AHL-producing bacteria are present in vacuum-packed meat during storage and spoilage, but AHL does not appear to influence the spoilage of this particular type of conserved meat. Our data indicate that AHL-producing H. alvei may induce food quality-relevant phenotypes in other bacterial species in the same environment. H. alvei may thus influence spoilage of food products in which Enterobacteriaceae participate in the spoilage process.

* Corresponding author. Mailing address: Danish Institute for Fisheries Research, Department of Seafood Research, Søltofts Plads, c/o Technical University of Denmark bldg. 221, DK-2800 Kgs. Lyngby, Denmark. Phone: 45 4525 2571. Fax: 45 4588 4774. E-mail: jbb{at}dfu.min.dk.

Applied and Environmental Microbiology, July 2004, p. 4293-4302, Vol. 70, No. 7
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.7.4293-4302.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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