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Spoilage of Vacuum-Packed Meats

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Spoilage of Vacuum-Packed Meats International Journal of Systematic Bacteriology (1 999), 49, 1 539-1 550 Printed in Great Britain Clostridiurn frigidicarnis sp. nov., a psychrotolerant bacterium associated with 'blown pack' spoilage of vacuum-packed meats D. M. Broda,'c2 P. A. Law~on,~R. G. Bell' and D. R. Musgrave' Author for correspondence: D. M. Broda. Tel: +64 7 854 8550. Fax: +64 7 854 8560. e-mail : [email protected] lr2 Department of Biological Two strains of a psychrotolerant Clostridiurn, isolated from vacuum-packed, Sciences, University of temperature-abused beef, were characterized using a multiphasic approach. Waikato', and MlRlNZ Food Technology & The strains were Gram-positive motile rods producing elliptical subterminal Research, PO Box 6172, spores during early stationary growth phase. The strains were psychrotolerant. Hamilton, New Zealand At pH 7.0, they grew between 3.8 and 40.5 "C; their optimum growth 3 Department of Food temperature was 3090-38-5"C. At 30 "C, the pH range for growth was between Science and Technology, University of Reading, 4.7 and 9.5; the optimum pH for growth was 64-7-2. The organisms were Reading RG6 6BZ, UK proteolytic and saccharolytic, lecithinase-positive and hydrolysed gelatin. The fermentation products formed in peptone/yeast extract/glucose/starch broth were acetate, ethanol, butyrate, isovalerate, butanol, isobutyrate, oxalacetate, lactate, hydrogen and carbon dioxide. The DNA G+C compositions of the two meat strains were 27.3 and 28.4 mol%. Phylogenetic analyses indicated that the strains belong to Cluster I of the genus Clostridium (sensu Collins et a/., 1994). The new strains differed from phylogenetically related clostridia in terms of cellular fatty acid composition, soluble protein profiles and phenotypic properties. On the basis of phenotypic and genotypic characterization data, the strains were assigned to a new species for which the name Clostridiurn frigidicarnis is proposed; strain SPL77Af (= DSM 12271') is the type strain. Keywords : Clostridium frigidicarnis, psychrotolerance, meat spoilage INTRODUCTION nized as the causative agents of 'blown pack ' spoilage of vacuum-packed meat (Dainty et al., 1989; Historically, Clostridium species were believed to play Kalchayanand et al., 1989; Broda et al., 1996). only a minor role in meat spoilage (Gill, 1979 ; Roberts Similarly, production of offensive, sickly odours in & Mead, 1986). Early reports (Ingram, 1952; Callow & vacuum-packed cooked pork has been attributed to Ingram, 1955 ; Ross, 1965) regarded mesophilic the growth of a psychrotolerant Clostridium species clostridia and Clostridium putrefaciens, which is atypi- (Lawson et al., 1994). These types of meat spoilage cal with respect to its growth temperature range, as the occur during chilled storage in the absence of tem- causative agents of deep tissue spoilage (' bone taint ') perature abuse. of beef and/or cured hams. Clostridium-mediated 'bone taint' spoilage was believed to have been To date, three psychrotolerant meat spoilage-causing eliminated by the development of chilled storage and species of clostridia have been described : Clostridium modern packaging technologies (Roberts & Mead, estertheticum (Collins et al., 1992), Clostridium 1986). However, more recently, psychrotolerant laramiense (Kalchayanand et al., 1993 ; Truper & De' Clari, 1997) and (Lawson (psychrophilic) Clostridium species have been recog- Clostridium algidicarnis et al., 1994). However, the results obtained from a slaughter stock survev that included faecal. hide and , , , , , , ,. , . , . , ,. , .. , . , , .. , . , . , . , ., . .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. (J. Abbreviations: CFA, cellular fatty acids; FAME, fatty acid methyl esters; **Boerema, D- M. Broda c!k R*G* FC. final concentration;.. FID. flame ionization detector. Bell, unpublished results), as well as examination of The GenBank accession number for the 165 rRNA gene sequence of strain spoiled iacuum packs (Broda al.7 1996), indicate SPL77AT is AF069742. that numerous species of psychrotolerant clostridia, 00996 0 1999 IUMS 1539 D. M. Broda and others including some spoilage-causing strains, may be com- 48 h. The morphology of well-isolated colonies was de- monly associated with slaughter stock and vacuum- scribed. packed meat. It appears, therefore, that the detection For descriptions of vegetative cell and spore morphology, of psychrotolerant Clostridium species as a group in meat strains were grown in PYGS broth at 30 "C for 18 h vacuum-packed meat may no longer be sufficient to and 5 d, respectively. A light microscope (Leitz Orthoplan) account for premature meat spoilage at refrigeration in phase-contrast mode was used to examine and photo- temperatures. Consequently, to effect spoilage control graph vegetative cells and spores of each bacterium. Presence it is necessary first to determine which clostridial of flagella was determined in 18-h-old cultures of strains species are causing the spoilage and second to trace the SPL77ATand SPL77B. For this determination, the cultures causative micro-organism back to its reservoir of were washed with water, allowed to settle onto Formvar- contamination in the meat plant. coated copper grids and negatively stained with 1-2 O/O (w/v) uranyl acetate (Beveridge et al., 1994). Stained grids were The aim of this study was to describe and characterize dried and examined with a transmission electron microscope a psychrotolerant Clostridium species associated with a (Philips EM 400). meat spoilage incident. These data may also provide a The ultrastructure of vegetative cells and spores was de- means to differentiate this new species from other termined for the isolates grown in PYGS broth at 30 "C for psychrotolerant clostridia, both spoilage-causing and 18 h and 5 d, respectively. The bacteria were fixed overnight benign, that may be encountered in spoiled vacuum at 4 "C in a solution containing 2.5 '/O (v/v) glutaraldehyde packs and the meat plant environment. Such differen- in 100 mM sodium cacodylate buffer (pH 7.2). The fixed cells tiation will facilitate tracing spoilage-causing clostridia were washed in 100 mM sodium cacodylate buffer and post- to their reservoirs within the abattoir. fixed with 1Yo (w/v) aqueous osmium tetroxide. The cells were then stained en bloc with 4% (w/v) aqueous uranyl acetate, dehydrated and embedded in Spurr embedding METHODS medium. Ultra-thin sections were then prepared and stained with a 4% (w/v) uranyl acetate and lead citrate solution General procedures. Unless stated otherwise, stringent an- (Beveridge et al., 1994). The grids containing sections were aerobic procedures (Holdeman et al., 1977) were used for examined with a transmission electron microscope. culturing all Clostridium strains and for physiological and substrate utilization tests. All anaerobic media that con- (ii) Gram reaction, Gram-type and cell wall type. Exponentially tained reducing agents were pre-reduced by cooling after growing (at 30 "C for 18 h) cells of strains SPL77AT and sterilization inside an anaerobic chamber (Forma Scientific) SPL77B were Gram stained using the method of Johnson et operating with an anaerobic gas mixture (10 YO,v/v Hz; 5 %, al. (1995). A KOH test (Powers, 1995) was additionally v/v CO,; 85%, v/v N,). Only fully reduced media, as conducted to determine the Gram-type of cells grown on the indicated by the colourless state of resazurin indicator in the surface of CBA with 5 % (v/v) sheep blood at 30 "C for 18 h. medium, were used for tests. Cell wall type was determined using transmission electron microscopy, as described in the previous section. Bacteria. Strains SPL77AT (T = type strain) and SPL77B were initially isolated from the same ' blown ' temperature- (iii) Physiological tests. For physiological tests, growth was abused vacuum pack of raw beef using methods described determined by monitoring an increase in OD550,as measured previously (Broda et al., 1996). After their initial isolation, with a spectrophotometer (Novaspec 11; Pharmacia), against strains SPL77AT and SPL77B were maintained as freeze- three uninoculated controls. dried cultures. Before characterization, both strains were revived from freeze-dried material in peptone/yeast extract/ The potential for growth at 25 pH values ranging from 4.23 to 9.82 was determined at 30 "C in peptone/yeast extract glucose/starch (PYGS) broth (Lund et al., 1990), sub- cultured onto Columbia Blood Agar (CBA; Oxoid) con- (PY) broth (Holdeman et al., 1977) with glucose con- taining 5% (v/v) sheep blood (Life Technologies) and centration adjusted to 0.5 '/O (w/v). Broths were inoculated incubated at 30 "C for 48 h. Strains were checked for purity with 2 YO(v/v) culture growing exponentially at pH 7.0. The before use. pH of the broth was kept constant (k0.1 unit) by adjustment with potassium phosphate buffer. The broth pH was Reference strains of Clostridium cadaveris (DSM 1284T), measured with a pH meter (Schott CG 837; Labsupply Clostridium fallax (DSM 263 lT), Clostridium intestinale Pierce) equipped with a combination electrode. Cultures (DSM 6191T) and Clostridium carnis (DSM 1293T) were were incubated for up to 10 d to determine whether growth obtained from the Deutsche Sammlung von Mikroorganis- occurred. men und Zellkulturen GmbH, Braunschweig, Germany. A reference strain of C. algidicarnis (NCFB 2931T) was Growth rates were measured for 43 temperatures ranging obtained from the National Collection of Food Bacteria, from - 1.5 to 47.0 "C. The temperature range for growth
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