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Psychrobacters and Related Bacteria in Freshwater Fish

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Psychrobacters and Related Bacteria in Freshwater Fish 315 Journal of Food Protection, Vol. 63, No. 3, 2000, Pages 315±321 Copyright Q, International Association for Food Protection Psychrobacters and Related Bacteria in Freshwater Fish CE SAR J. GONZA LEZ, JESU S A. SANTOS, MARIÂA-LUISA GARCIÂA-LO PEZ,* AND ANDRE S OTERO Department of Food Hygiene and Food Technology, Veterinary Faculty, University of LeoÂn, E-24071-LeoÂn, Spain MS 99-109:Received 27 April 1999/Accepted 7 October 1999 ABSTRACT Three phenotypic identi®cation systems were employed to identify 106 strains of gram-negative, nonmotile, aerobic Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/3/315/1673422/0362-028x-63_3_315.pdf by guest on 29 September 2021 bacteria obtained during iced storage of wild (Salmo trutta and Esox lucius) and farmed (Oncorhynchus mykiss) freshwater ®sh. Using diagnostic tables and computer-assisted identi®cation, the isolates were Psychrobacter (64 strains), Acinetobacter (24 strains), Moraxella (6 strains), Chryseobacterium (5 strains), Myroides odoratus (2 strains), Flavobacterium (1 strain), Empedobacter (1 strain), and unidenti®ed (3 strains). Overall similarities of all strains were determined for 108 characters by numerical analysis (simple matching coef®cient of similarity [S] and clustering by unweighted pair group average linkage [UPGMA]). At the 77% similarity level, 92 strains formed nine major clusters (3 or more strains) and four small clusters (2 strains). Cluster 1 (25 isolates divided into two main subclusters) could be assigned to Psychrobacter phenylpyruvicus, clusters 2 and 3 (26 isolates) were designated as Psychrobacter immobilis, and clusters 4 (3 isolates) and 7 (4 isolates) were identi®ed as Psychrobacter urativorans and Psychrobacter spp., respectively. Clusters 5 (®ve isolates), 6 (three isolates), and 9 (®ve isolates) were labeled as Acinetobacter spp., Acinetobacter johnsonii, and Acinetobacter lwof®i, respectively. Cluster 8 (12 isolates), with a high resemblance to Thornley's phenon 4 (a heterogeneous group of bacteria isolated from poultry and related to Acinetobacter), remained unnamed. The restriction pattern was identical for strains grouped into clusters 2 and 3 (P. immobilis) but was different for the remaining Psychrobacter isolates. A large proportion of isolates belonging to the family Moraxellaceae were closely related. Psychrobacters and A. johnsonii were present in freshly caught ®sh and river water. In the latter stages of storage, P. phenylpyruvicus and acinetobacters tended to decrease, whereas P. immobilis increased. Spoilage of chilled raw ®sh stored in air is a result of ice, and samples from the three latter sampling sites were taken enzymatic changes (autolysis), nonenzymatic reactions at regular intervals (days 3, 6, 9, 12, and 15). Rainbow trout spec- (rancidity), and metabolic activity of bacteria, the latter be- imens were collected from two commercial ®sh farms located on  ing particularly important (7). Although available infor- river systems (Duerna and Orbigo; water temperature between 7 8 mation on spoilage bacteria of freshwater ®sh is limited, it and 11 C) within the province of LeoÂn (northwest of Spain) dur- appears that, like in marine ®sh, Pseudomonas spp. are ing April to July 1997. Wild brown trout specimens, provided by one ¯y ®sherman, also were caught during April through July dominant (13, 15, 38). Gram-negative, nonmotile, aerobic 1997 in nine rivers (Selmo, Eria, Esla, CuruenÄo, TorõÂo, Sil, Burbia, rods and coccobacilli, identi®ed as acinetobacters, morax- Porma, and O rbigo; water temperature between 5 and 158C) of ellae, psychrobacters (Moraxella-like), and ¯avobacteria, the same province. Pike was obtained from Esla and Porma rivers also occur but their relative incidence and role in spoilage (water temperature between 8 and 128C). are dif®cult to establish due, in part, to their confusing clas- Water samples (200 ml) were collected simultaneously with si®cation and the consequent misidenti®cation (10). the ®sh from approximately a 50-cm depth using a sterile glass The aim of this work was to identify the genera and bottle. species of gram-negative, nonmotile, aerobic bacteria that were associated with freshwater ®sh and their surrounding Strains. Tryptone soya agar (Oxoid, Basingstoke, UK) was environment in accordance with the new classi®cations. used to count aerobic mesophilic ¯ora at 308C for 2 days and The behavior of these organisms during storage and their aerobic psychrotrophic ¯ora at 78C for 10 days. A Harrison disk spoilage potential are also discussed. (16) was used for random selection of 979 strains. The 106 strains (50 mesophiles and 56 psychrotrophs) included in this study were MATERIALS AND METHODS the aerobic, gram-negative, nonmotile bacilli and coccobacilli found among this population. Inocula for tests were grown in tryp- Samples. Ten lots (three specimens each) of farmed rainbow tone soya broth (Oxoid) for 24 to 36 h at 258C. Control plates trout (Oncorhynchus mykiss), 10 lots of wild brown trout (Salmo with tryptone soya agar were used to ensure viability and purity trutta), and 4 lots of wild pike (Esox lucius) were studied. Freshly caught or collected ®sh were sampled at the following sites: gills, of inocula. intestines, surface of skin, muscle, and surface of the body cavity. The following reference strains were included in the numer- Surfaces of skin and the body cavity were sampled by scraping ical analysis: Myroides odoratus CECT 998 (Spanish Type Cul- and rinsing; gills, intestine, and muscle were aseptically excised ture Collection, Universidad de Valencia, Spain), Moraxella os- with a scalpel. Afterwards, the specimens were stored in melting loensis CECT 460, Acinetobacter calcoaceticus CECT 441, and Psychrobacter immobilis ATCC 43116. Type strains used as the * Author for correspondence. Tel: 134-987-291119; Fax: 134-987- biological controls for tests were those recommended by Lanyi 291284; E-mail: [email protected]. (24). 316 GONZA LEZ ET AL. J. Food Prot., Vol. 63, No. 3 Phenotypic tests. Unless otherwise stated, cultures were in- cording to Sneath and Johnson (32). Separation indexes were cal- cubated at 25 6 18C. The following tests were performed, as culated according to Sneath (31). previously described (9, 23): morphology; arrangement and Gram reaction; motility; colony appearance and pigmentation; pyoverdin Ampli®ed ribosomal DNA restriction analysis of Psychro- and pyocyanin production; ability to grow at 4, 35, and 428C; salt bacter strains. Representative strains of the different clusters of tolerance (3 and 6% NaCl); growth at pH 4.5; growth on selective Psychrobacter (I, II, III IV, and VII; see Results) were cultured media (MacConkey agar, Simmon's citrate agar, and thiosulphate in tryptone soya broth, and DNA was extracted by a standard citrate bile salts sucrose agar); oxidase and catalase production; procedure (25). The 16S ribosomal DNA gene was ampli®ed by hemolytic activity on sheep blood; sensitivity to penicillin (1 IU polymerase chain reaction using primers pA and pH* (18) in a ml21) and vibriostatic agent O/129 (150 mg); reduction of nitrate Mastercycler Personal thermal cycler (Eppendorf). Each ampli®- 8 and trimethylamine N-oxide (Sigma); urease production; decar- cation cycle consisted of denaturation for 30 s at 92 C, annealing for30sat558C, and extension for 1 min at 728C, followed by a boxylation of L-lysine and L-ornithine; arginine dihydrolase; de- 8 m composition of hippurate; production of indole; esculin hydroly- ®nal extension cycle of 2 min at 72 C. Approximately 2 gof the ampli®ed products (ca. 1.5 kb in length) was digested with 10 sis; H2S production from cysteine; hydrolysis of tyrosine, DNA, 8 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/3/315/1673422/0362-028x-63_3_315.pdf by guest on 29 September 2021 gelatin, casein, elastin, and starch; production of levan from su- UofHaeIII (Sigma) for6hat37C. The digestion products were crose; methyl red and Voges-Proskauer reactions; gluconate oxi- electrophoretically separated in a 2% agarose gel, stained with ethidium bromide, and viewed under UV light. dation; gas production from glucose; o-nitrophenyl-b-D-galacto- pyranoside; lipolytic activity on Tween 20, Tween 80, tributyrin, RESULTS and egg yolk; acid production from carbohydrates (adonitol, L- arabinose, cellobiose, D-fructose, D-galactose, glycerol, glucose, Using diagnostic tables (1, 3, 4, 8, 21, 27, 35, 36) and meso-inositol, lactose, maltose, D-mannitol, D-mannose, melibi- the probability matrix (computer-assisted identi®cation ose, raf®nose, L-rhamnose, D-ribose, salicin, sorbitol, L-sorbose, (27)), 101 isolates were allocated to six genera: Psychro- sucrose, starch, trehalose, xylitol, and D-xylose); and assimilation bacter (64 strains), Acinetobacter (24 strains), Moraxella (6 of sole carbon sources (adonitol, D-arabinose, L-arabinose, cello- strains), Chryseobacterium (5 strains), Empedobacter (1 biose, D-fructose, D-galactose, glycerol, D-glucose, D-gluconate, strain), and Flavobacterium (1 strain). Three strains were meso-inositol, lactose, maltose, D-mannitol, D-mannose, L-rham- not identi®ed to the genus level, and two strains were iden- nose, salicin, sorbitol, sucrose, starch, trehalose, xylitol, n-butanol, ti®ed as Myroides odoratus. ethanol, L-arginine, L-cysteine, L-lysine, glycine, and sodium for- mate). The average probability of error (P) was 3.4%, which would not produce important distortion of the taxonomic Taxonomic schemes. Conventional tests employed for the structure. The cophenetic correlation value was 0.816. At identi®cation of the strains were mainly those recommended by the 77% similarity level (S), 92 strains (90 isolates and 2 Doern (8), Juni (21), Prieto et al. (28), Towner (36), Vandamme reference strains) formed 13 clusters (Fig. 1), 9 of them et al. (37), Bernardet et al. (1), and Bowman et al. (3, 4). containing 3 or more strains. There were four small clusters Computer-assisted identi®cation. A probability matrix for (2 strains) and 18 unclustered strains, of which 2 were ref- the identi®cation of species of gram-negative, nonmotile, aerobic erence and 16 were ®eld strains. Cluster 1 could be as- bacteria constructed by Prieto (27) was also used.
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