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Int J Syst Evol Microbiol 56 (2006), 1317-1322; DOI  10.1099/ijs.0.64014-0
© 2006 International Union of Microbiological Societies

Chryseobacterium piscium sp. nov., isolated from fish of the South Atlantic Ocean off South Africa

Hanli de Beer1, Celia J. Hugo2, Piet J. Jooste3, Marc Vancanneyt4, Tom Coenye5 and Peter Vandamme5

1 School for Agriculture and Environmental Science, Central University of Technology: Free State, 1 President Brandt Street, Bloemfontein 9300, South Africa
2 Department of Microbial, Biochemical and Food Biotechnology, University of the Free State, Bloemfontein, South Africa
3 Department of Biotechnology and Food Technology, Tshwane University of Technology, Pretoria, South Africa
4 BCCM/LMG Bacteria Collection, Ghent University, K. L. Ledeganckstraat 35, Ghent B-9000, Belgium
5 Laboratorium of Microbiology, Ghent University, K. L. Ledeganckstraat 35, Ghent B-9000, Belgium

Correspondence
Hanli de Beer
hdebeer{at}cut.ac.za


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Four isolates from freshly caught fish samples obtained from the South Atlantic Ocean off the South African coastline were shown to represent a novel species in the genus Chryseobacterium by means of a polyphasic taxonomic study. The four isolates had virtually identical whole-cell protein profiles, fatty acid profiles and biochemical properties. Analysis of the 16S rRNA sequence of strain LMG 23089T revealed 99.3 and 98.9 % similarity to the 16S rRNA sequences of the type strains of Chryseobacterium balustinum and Chryseobacterium scophthalmum, respectively. Strain LMG 23089T and the C. balustinum and C. scophthalmum type strains formed a stable lineage supported by a bootstrap value of 100 %. The levels of DNA–DNA hybridization towards these nearest phylogenetic neighbours were below 57 %. The absence of growth on MacConkey agar or at 37 °C (on nutrient agar), the capacity to grow in the presence of 5 % NaCl and the production of urease activity differentiate this novel taxon from C. balustinum and C. scophthalmum. The four isolates are formally classified as Chryseobacterium piscium sp. nov., with strain LMG 23089T (=CCUG 51923T) as the type strain. Its DNA G+C content is 33.6 mol%.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Chryseobacterium piscium LMG 23089T is AM040439.


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Apart from being a source for several food-borne pathogens like Salmonella and Vibrio species and Listeria monocytogenes, raw fish, a protein-rich food with a neutral pH (6.6–6.8) and high water activity, is a suspected source for microbial growth and deterioration. The combination of a high water content and the composition of the flesh enhance rapid spoilage in comparison with other types of raw meat (Sato, 2004Go). Psychrotolerant, Gram-negative bacteria dominate the spoilage flora, members of the family Pseudomonadaceae being major spoilage organisms (Forsythe, 2000Go). Rapid changes in the taxonomy of the family Flavobacteriaceae during the past decade and the description of Chryseobacterium joostei, isolated from milk (Hugo et al., 2003Go), initiated a long-term investigation into the incidence of yellow-pigmented colonies on raw fish. Chryseobacterium species inhabit water, soil and the clinical environment, but are also recovered from food sources, such as milk, meat, poultry and fish (Vandamme et al., 1994Go; Jooste & Hugo, 1999Go; Hugo et al., 2003Go; Kämpfer et al., 2003Go; Li et al., 2003Go; Pavlov et al., 2004Go).

Potential Chryseobacterium isolates were obtained from fresh fish from the South Atlantic Ocean in the course of 1996 and were analysed by whole-cell protein electrophoresis. A cluster of four isolates collected in February (LMG 23086), June (LMG 23087) and July (LMG 23088 and LMG 23089T) of that year differed from Chryseobacterium reference strains and prompted the taxonomic study reported herein. Reference strains from established Chryseobacterium species and related bacteria were available from the BCCM/LMG Bacteria Collection (Ghent University, Ghent, Belgium). After growth for 24 h on tryptic soy agar (BBL), cells were harvested and whole-cell protein extracts were prepared and subjected to whole-cell protein electrophoresis as described by Pot et al. (1994)Go. A densitometric analysis, normalization and interpolation of the protein profiles and a numerical analysis were performed by using the GelCompar software package (Applied Maths). The four isolates had virtually identical whole-cell protein profiles (the correlation level was above 0.96), which were most similar to those of the Chryseobacterium balustinum and Chryseobacterium indoltheticum type strains (correlation levels of 0.91 and 0.89, respectively) (Fig. 1Go).


Figure 1
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  		Fig. 1. Dendrogram derived from the unweighted pair group average linkage of correlation coefficients between the whole-cell protein profiles of the novel strains (Chryseobacterium piscium sp. nov.) and reference strains of related taxa. Protein profiles were reproduced using the GelCompar software package. For convenience, the correlation coefficient is expressed as percentage similarity. The grey bar in the marker lane indicates the part of the protein profile that was used in the numerical analysis.

 
High-molecular-mass DNA of strain LMG 23089T and of Chryseobacterium reference strains was prepared according to Pitcher et al. (1989)Go. In order to determine the phylogenetic position of this taxon, the 16S rRNA gene sequence of LMG 23089T was determined as described by Willems et al. (2003)Go and analysed by using the BioNumerics 4.0 (Applied Maths) software package. A phylogenetic tree (Fig. 2Go) was constructed using the neighbour-joining method. The 16S rRNA gene sequence of LMG 23089T showed 99.3, 98.9 and 97.4 % similarity to the corresponding gene sequences of the type strains of C. balustinum, Chryseobacterium scophthalmum and C. indoltheticum, respectively. Strain LMG 23089T and the C. balustinum and C. scophthalmum type strains formed a stable lineage characterized by a bootstrap value of 100 % (Fig. 2Go). The sequence similarity values with respect to the other type strains were below 97 %.


Figure 2
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  		Fig. 2. Neighbour-joining phylogenetic tree of C. piscium sp. nov. LMG 23089T and related bacteria, based on 16S rRNA gene sequence comparisons. Bootstrap values above 60 % (obtained with 1000 repetitions) are indicated. The 16S rRNA gene sequence of Ornithobacterium rhinotracheale LMG 9086T was included as the outgroup. Bar, 1 % sequence divergence.

 
DNA–DNA hybridizations were performed with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989)Go, using an HTS7000 Bio Assay Reader (Perkin Elmer) for the fluorescence measurements. The hybridization temperature was 33 °C. In order to determine the G+C content (mol%) of strain LMG 23089T, DNA was enzymically degraded into nucleosides as described by Mesbah et al. (1989)Go. The obtained nucleoside mixture was then separated by HPLC using a Waters SymmetryShield C8 column regulated at 37 °C. The solvent was 0.02 M NH4H2PO4 (pH 4.0) with 1.5 % acetonitrile. Non-methylated {lambda} phage DNA (Sigma) was used as the calibration reference. The detector used was a Waters model 484 UV-VIS absorbance detector set at 270 nm. DNA–DNA hybridizations between strain LMG 23089T and the type strains of C. balustinum, C. scophthalmum and C. indoltheticum yielded binding values of 57, 51 and 52 %, respectively. The DNA G+C content of LMG 23089T was 33.6 mol%, which corresponds with the range (34–38 mol%) for the genus Chryseobacterium (Vandamme et al., 1994Go).

Whole-cell fatty acid components of the four strains were prepared from a loopful of well-grown cells that had been incubated for 24 h at 28 °C. Fatty acid profiles were generated under highly standardized conditions, as previously described by Vandamme et al. (1992)Go. Separation and identification of esters were done with the Sherlock Microbial Identification System (MIDI, version 3.0). Mean percentages and standard deviations were calculated. Table 1Go gives a summary of the fatty acid composition of the tested strains in comparison with those of the other Chryseobacterium reference strains. The mean percentages of the predominant fatty acids were as follows: iso-C15 : 0, 38.3 %; iso-C17 : 1{omega}9c, 18.7 %; iso-C17 : 0 3-OH, 16.2 %; and summed feature 3, 10.8 %.


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  		Table 1. Fatty acid compositions of Chryseobacterium and Elizabethkingia species

Species: 1, C. piscium sp. nov. (n=4; data from this study); 2, C. indoltheticum (n=1); 3, C. balustinum (n=1); 4, C. gleum (n=5); 5, C. indologenes (n=45); 6, C. scophthalmum (n=2); 7, C. joostei (n=11) (data in columns 2–7 from Hugo et al., 2003Go); 8, C. defluvii (n=1) (Kämpfer et al., 2003Go); 9, C. formosense (n=1) (Young et al., 2005Go); 10, C. daecheongense (n=1) (Kim et al., 2005Go); 11, C. taichungense (n=1) (Shen et al., 2005Go); 12, C. shigense (n=1) (Shimomura et al., 2005Go); 13, C. vrystaatense (n=7) (de Beer et al., 2005Go); 14, Elizabethkingia meningoseptica (n=1) (Hugo et al., 2003Go); 15, Elizabethkingia miricola (n=1) (Li et al., 2003Go). Values are percentages of total fatty acids; values derived from more than one strain are means±SD. Symbols: tr, trace amounts (<1 %); ND, not detected; NA, data not available; ECL, equivalent chain length (i.e. the identity of the fatty acid is unknown).

 
A detailed phenotypic characterization of the four isolates was subsequently performed by using conventional biochemical techniques and the Biolog GN2 MicroPlate method. Data for other Chryseobacterium reference strains were obtained from a previous study (de Beer et al., 2005Go). A 24 h culture, incubated at 25 °C, was suspended in quarter-strength Ringer's solution to give a McFarland Barium Sulphate Standard 2 suspension. A battery of tests was selected to differentiate the species in the genus according to the methods described by Cowan (1974)Go, MacFaddin (1980)Go, Gerhardt et al. (1981)Go and Hugo et al. (2003)Go, along with the Biolog GN2 MicroPlate, which was used according to the manufacturer's protocol. Test results are shown below in the species description and in Table 2Go, which includes the biochemical tests useful for the differentiation of the novel species from established Chryseobacterium species; specific phenotypic tests were performed as described by Hugo et al. (2003)Go. The present data demonstrated that these four isolates from raw fish represent a novel species, for which we propose the name Chryseobacterium piscium.


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  		Table 2. Phenotypic properties that differentiate C. piscium sp. nov. from other Chryseobacterium and Elizabethkingia species

Data were obtained in this study unless indicated otherwise. Species: 1, C. piscium sp. nov. (n=4); 2, C. indoltheticum (n=1); 3, C. balustinum (n=1); 4, C. gleum (n=1); 5, C. indologenes (n=1); 6, C. scophthalmum (n=1); 7, C. joostei (n=1); 8, C. defluvii (n=1); 9, C. formosense(n=1) (data from Young et al., 2005Go); 10, C. daecheongense (n=1) (Kim et al., 2005Go); 11, C. taichungense (n=1) (Shen et al., 2005Go); 12, C. shigense (n=1) (Shimomura et al., 2005Go); 13, C. vrystaatense (n=36); 14, E. meningoseptica (n=1); 15, E. miricola (n=1) (Liet al., 2003Go). Symbols: +, positive; w, weakly positive; –, negative; V, variable reaction; D, delayed; NA, no data available. Phenotypic tests were done as described by Hugo et al. (2003)Go.

 
Description of Chryseobacterium piscium sp. nov.
Chryseobacterium piscium (pis'ci.um. L. pl. gen. n. piscium of fish).

Colonies are shiny, yellow and translucent with entire edges. Cells are rod-shaped and the cell dimensions are approximately 1.0 µm by <0.5 µm (Fig. 3Go). Cells are Gram-negative, catalase- and oxidase-positive and produce flexirubin pigment in the presence of 20 % KOH. They produce an alkaline reaction in the oxidation–fermentation test. Colonies form after 24 h at 4, 15, 25 and 32 °C. Very weak growth occurs on nutrient agar but not at 37 or 42 °C or on MacConkey no. 3 (Oxoid CM115) agar. Grows in nutrient broth with a 5 % NaCl solution. Aesculin production occurs within 4 h. Strains test positive for phenylalanine deaminase activity, gelatin hydrolysis, casein hydrolysis, lecithinase and phosphatase activity and produce urea from ammonia. Weak DNase activity occurs but there is no starch or tyrosine hydrolysis. Reaction on triple-sugar iron agar (Oxoid CM277) and 10 % lactose is alkaline and strains do not produce H2S from triple-sugar iron agar or SIM medium (Oxoid CM435). The ability of the strains to oxidize a panel of 95 different carbon sources was tested with the Biolog system: only four positive reactions were encountered in all four isolates, namely metabolism of gentiobiose, D-mannose, succinic acid monomethyl ester and acetic acid.


Figure 3
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  		Fig. 3. Transmission electron micrograph of a cross-section of cells of C. piscium sp. nov. LMG 23089T. Bar, 500 nm.

 
The type strain is LMG 23089T (=CCUG 51923T). All currently known strains were isolated from fresh fish caught in the South Atlantic Ocean off the South African coastline during 1996. The production of urea and phenylalanine deaminase suggests that C. piscium may be involved in spoilage. Three additional isolates have been deposited in the BCCM/LMG Bacteria Collection as LMG 23086, LMG 23087 and LMG 23088.


   ACKNOWLEDGEMENTS
 
We are indebted to the National Research Foundation, South Africa (H. de B.), and the Fund for Scientific Research – Flanders (Belgium) for a position as postdoctoral fellow (T. C.) and research grants (P. V.), respectively. We also wish to acknowledge Dr A. Jacoby (Central University of Technology, Bloemfontein, South Africa) and the Centre for Confocal and Electron Microscopy (University of the Free State, Bloemfontein, South Africa) for the transmission electron microscope image.


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Hugo, C. J., Segers, P., Hoste, B., Vancanneyt, M. & Kersters, K. (2003). Chryseobacterium joostei sp. nov., isolated from the dairy environment. Int J Syst Evol Microbiol 53, 771–777.[Abstract/Free Full Text]

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MacFaddin, J. F. (1980). Biochemical Tests for Identification of Medical Bacteria, 2nd edn. Baltimore: Williams & Wilkins.

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