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Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Guseong 373-1, Yuseong, Daejeon 305-701, Korea
Correspondence
Sung-Taik Lee
e_stlee{at}kaist.ac.kr
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) Vandamme et al. 1994 and the type strain of Chryseobacterium miricola Li et al. 2004 were re-evaluated by using a polyphasic taxonomic approach. Phylogenetic analysis, based on 16S rRNA gene sequencing, showed that the strains represent a separate lineage from the type strains of the Chryseobacterium–Bergeyella–Riemerella branch within the family Flavobacteriaceae (90·7–93·9 % similarities), which was supported by phenotypic differences. Combined phylogenetic and phenotypic data showed that C. meningosepticum and C. miricola should be transferred to a new genus, Elizabethkingia gen. nov., with the names Elizabethkingia meningoseptica comb. nov. (type strain, ATCC 13253T=NCTC 10016T=LMG 12279T=CCUG 214T) and Elizabethkingia miricola comb. nov. (type strain, DSM 14571T=JCM 11413T=GTC 862T) proposed.
Published online ahead of print on 14 January 2005 as DOI 10.1099/ijs.0.63541-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Elizabethkingia meningoseptica ATCC 13253T and Elizabethkingia miricola GTC 862T are AJ704540 and AB071953, respectively.
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; Bernardet et al., 1996). At that time the genera Chryseobacterium (including six species previously considered Flavobacterium species, Chryseobacterium balustinum, Chryseobacterium gleum, Chryseobacterium indologenes, Chryseobacterium indoltheticum, Chryseobacterium meningosepticum and Chryseobacterium scophthalmum), Bergeyella (including a single species, Bergeyella zoohelcum, previously considered a Weeksella species) and Riemerella (including a single species, Riemerella anatipestifer, long considered a Moraxella species) composed a separate rRNA branch of the family Flavobacteriaceae in rRNA superfamily V. Although ‘Chryseobacterium proteolyticum’ (Yamaguchi & Yokoe, 2000), Chryseobacterium defluvii (Kämpfer et al., 2003), Chryseobacterium joostei (Hugo et al., 2003), Chryseobacterium miricola (Li et al., 2003) and Riemerella columbina (Vancanneyt et al., 1999) have been described since then, the Chryseobacterium–Bergeyella–Riemerella (CBR) branch retains its original taxonomic position. However, recent 16S rRNA gene sequence similarity studies have revealed that the genus Chryseobacterium is genetically heterogeneous, and that C. meningosepticum and C. miricola can be readily differentiated from other Chryseobacterium species.
The aim of this study was to clarify the taxonomic positions of six strains of C. meningosepticum (King 1959) Vandamme et al. 1994 and C. miricola Li et al. 2004 within the family Flavobacteriaceae by using a polyphasic approach.
Strains used in this study are listed in Table 1. All were cultivated on nutrient agar (Difco) at 28 °C except the two Riemerella strains, which were cultivated on trypticase soy agar (TSA; BBL) at 37 °C microaerobically. For analysis of fatty acids, all strains were cultivated on TSA for 24 h for direct comparison.
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. Cell morphology was observed under a phase-contrast microscope (1000x magnification; Nikon), with cells grown for 3 days on nutrient agar. Flexirubin-type pigment was detected with 20 % KOH according to the method of Fautz & Reichenbach (1980). Oxidase activity was tested using Bactident-Oxidase strips (Merck) and catalase activity was tested using 3 % H2O2. Growth was investigated at different temperatures (5, 37 and 42 °C), and on MacConkey agar, casein agar and starch agar (Difco). Acid production tests from sugar were performed as described by Yamaguchi & Yokoe (2000). Additional tests were performed using API 20NE, API 20E and API ZYM galleries according to the manufacturer's instructions (bioMérieux).
Fatty acid methyl esters were prepared and analysed as described by Klatte et al. (1994) using the standard Microbial Identification System (MIDI) for automated gas chromatographic analyses (Sasser, 1990; Kämpfer & Kroppenstedt, 1996).
Isoprenoid quinones were extracted and purified as described by Tindall (1990); dried preparations were dissolved in 200 µl of 2-propanol and 1 to 10 µl was separated by HPLC without further purification. Menaquinones were separated by HPLC on a COSMOSIL 5C18-MS column (nacalai tesque) at 40 °C using acetonitrile/2-propanol (65 : 35, v/v) as solvent (Kroppenstedt, 1982, 1985).
Chromosomal DNA was extracted and purified by using the DNeasy Tissue Kit and Genomic-tip system 100/G (Qiagen). In vitro amplification of extracted 16S rRNA genes was performed as described by Yoon et al. (1997) with some modifications. The 16S rRNA gene sequences were aligned with published sequences retrieved from EMBL by using CLUSTAL_X (Thompson et al., 1997) and edited using BioEdit (Hall, 1999). A phylogenetic tree was constructed on the basis of the neighbour-joining method (Saitou & Nei, 1987); evolutionary distances were estimated by the method of Jukes & Cantor (1969) using MEGA version 2.1 (Kumar et al., 2001).
DNA base composition (G+C content) was determined by HPLC after hydrolysis as described by Tamaoka & Komagata (1984) and non-methylated 
DNA (Sigma) was used as a reference standard. DNA–DNA hybridization to determine genomic relatedness was performed fluorometrically by the method of Ezaki et al. (1989) using photobiotin-labelled DNA probes and microdilution wells.
Six strains formerly classified as C. meningosepticum and the type strain of C. miricola formed visible colonies (diameter of 1·0–1·5 mm) on nutrient agar within 24 h. Good growth was observed on TSA and nutrient agar at 28–37 °C, but no growth was observed at 5 or 42 °C after 2 weeks. Most strains could grow on MacConkey agar. Colonies were white–yellow, translucent and shiny with entire edges, becoming mucoid after 3 days incubation. Flexirubin-type pigment was not detected and acid was produced from lactose, in contrast to other Chryseobacterium species. Nitrate was not reduced as an electron acceptor and malonate was not utilized as a carbon source. As determined with the API ZYM system, a wide spectrum of substrates could be hydrolysed. Physiological and biochemical characteristics that differentiate these strains from the type strains of the CBR branch are summarized in Table 2 and Table 3.
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). The fatty acids 15 : 0 iso, 17 : 0 iso 3-OH and summed feature 4 (15 : 0 iso 2-OH and/or 16 : 1
7c/t) were predominant and only the C. defluvii type strain showed similar profiles within the CBR branch.
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) they formed a clade that was distinct from related genera within the family Flavobacteriaceae and that could be divided into two different groups: a cluster of five strains (ATCC 13253T, ATCC 13254, ATCC 13255, ATCC 49470 and ATCC 51720), including the C. meningosepticum type strain, showing 98·2–100 % 16S rRNA gene sequence similarity with each other; and a cluster of two strains (DSM 14571T and ATCC 33958), including the C. miricola type strain, showing 99·5 % similarity with each other. Five strains of C. meningosepticum showed 97·8–98·4 % similarities to two strains of C. miricola.
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) and in turn these two C. miricola strains showed levels of DNA–DNA hybridization of 23–54 % to five strains of C. meningosepticum. By contrast, C. meningosepticum ATCC 13253T showed a DNA–DNA hybridization level of only 31–35 % to the remaining four strains of C. meningosepticum, levels among these latter four being 90–100 %. This genetic heterogeneity using DNA–DNA hybridization was reported by Ursing & Bruun (1987). In their studies, [Flavobacterium] meningosepticum could be divided into two genomic groups; group I (including the type strain) showed about 40–55 % DNA–DNA hybridization to group II. Subsequent studies investigating the phenotypic characterization and antimicrobial susceptibility of [F.] meningosepticum showed no characteristics differentiating the two genomic groups (Bruun & Ursing, 1987; Bruun, 1987). We detected no phenotypic or ecological differences among the five C. meningosepticum strains and therefore a proposal for a novel binomial name for the second genomovar within this species is not warranted. Combined phylogenetic and phenotypic data show that C. meningosepticum and C. miricola should be transferred to a new genus, Elizabethkingia gen. nov., with the names Elizabethkingia meningoseptica comb. nov. and Elizabethkingia miricola comb. nov. proposed.
Description of Elizabethkingia gen. nov.
Elizabethkingia (E.liz.a.beth.kin'gi.a. N.L. fem. n. Elizabethkingia in honour of Elizabeth O. King, who first described bacteria associated with infant meningitis, notably [Flavobacterium] meningosepticum in 1959).
Cells are Gram-negative, non-motile, non-spore-forming rods (0·5x1·0–2·5 µm). Good growth is observed on TSA and nutrient agar at 28–37 °C, but no growth is observed at 5 or 42 °C. Colonies are white–yellow, non-pigmented, semi-translucent, circular and shiny with entire edges. Catalase, oxidase, phosphatase and 
-galactosidase activities are positive. H2S is not produced. Casein, aesculin and gelatin are hydrolysed, but starch is not. Malonate is not utilized. Nitrate is not reduced. Acid is produced from D-fructose, D-glucose, lactose, D-maltose, D-mannitol and trehalose, but not from L-arabinose, D-cellobiose, raffinose, sucrose, salicin or D-xylose. As determined with the API ZYM system, the following substrates are hydrolysed: 2-naphthyl phosphate (pH 8·5), 2-naphthyl caprylate, L-leucyl-2-naphthylamide, L-valyl-2-naphthylamide, N-benzoyl-DL-arginine-2-naphthylamide, 2-naphthyl phosphate (pH 5·4), naphthol-AS-BI-phosphate, 2-naphthyl 
-D-glucopyranoside and 1-naphthyl-n-acetyl--D-glucosaminide, but the following substrates are not hydrolysed: 2-naphthyl myristate, naphthol-AS-BI--D-glucuronide, 6-bromo-2-naphthyl--D-glucopyranoside and 6-bromo-2-naphthyl--D-mannopyranoside. The fatty acid profile consists largely of 15 : 0 iso, 17 : 0 iso 3-OH and summed feature 4 (15 : 0 iso 2-OH and/or 16 : 17c/t). Menaquinone MK-6 is the predominant quinone. The G+C content of the DNA is 35·0–38·2 mol%.
The type species is Elizabethkingia meningoseptica.
Description of Elizabethkingia meningoseptica comb. nov.
Elizabethkingia meningoseptica (me.nin.go.sep'ti.ca. Gr. n. meninx, meningos meninges, membrane covering the brain; Gr. adj. septikos putrefactive; N.L. fem. adj. meningoseptica apparently referring to association of the bacterium with both meningitis and septicaemia, but not septic meningitis as the name implies).
Basonym: Flavobacterium meningosepticum King 1959 (Approved Lists 1980).
Cells are Gram-negative, non-motile, non-spore-forming rods (0·5x1·0–2·0 µm). Growth on MacConkey agar is strain-dependent. Indole is produced. Urea is not hydrolysed. Acid is produced from D-fructose, ethanol, D-glucose, glycerol, lactose, D-maltose, D-mannitol and trehalose, but not from L-arabinose, D-cellobiose, raffinose, sucrose, salicin or D-xylose. As determined with the API ZYM system, the following substrates are hydrolysed: 2-naphthyl phosphate (pH 8·5), 2-naphthyl caprylate, L-leucyl-2-naphthylamide, L-valyl-2-naphthylamide, N-benzoyl-DL-arginine-2-naphthylamide, 2-naphthyl phosphate (pH 5·4), naphthol-AS-BI-phosphate, 2-naphthyl--D-glucopyranoside and 1-naphthyl-N-acetyl--D-glucosaminide, but the following substrates are not hydrolysed: 2-naphthyl butyrate, 2-naphthyl myristate, naphthol-AS-BI--D-glucuronide, 6-bromo-2-naphthyl--D-glucopyranoside and 6-bromo-2-naphthyl--D-mannopyranoside. The fatty acid profile consists largely of 15 : 0 iso (43·9±2·0 %), 17 : 0 iso 3-OH (14·6±1·0 %) and summed feature 4 (15 : 0 iso 2-OH and/or 16 : 17c/t; 19·6±1·0 %). The G+C content of the DNA is 37·2±0·6 mol% (37·1 mol% for the type strain).
The type strain is ATCC 13253T (=NCTC 10016T=LMG 12279T=CCUG 214T).
Description of Elizabethkingia miricola comb. nov.
Elizabethkingia miricola [mi.ri'co.la. N.L. neut. n. mirum derived from mir (peace) (name of Russian space station); L. suff. -cola from L. masc. or fem. n. incola inhabitant; N.L. masc. or fem. n. miricola inhabitant of the Mir space station].
Basonym: Chryseobacterium miricola Li et al. 2004.
Cells are Gram-negative, non-motile, non-spore-forming rods (0·5x1·0–2·5 µm). Good growth is observed on MacConkey agar. Colonies are very sticky on solid medium. Indole is produced. Urea is hydrolysed. Acid is produced from D-fructose, D-glucose, lactose, D-maltose, D-mannitol and trehalose, but not from L-arabinose, D-cellobiose, raffinose, sucrose, salicin or D-xylose. As determined with the API ZYM system, the following substrates are hydrolysed: 2-naphthyl phosphate (pH 8·5), 2-naphthyl butyrate, 2-naphthyl caprylate, L-leucyl-2-naphthylamide, L-valyl-2-naphthylamide, L-cystyl-2-naphthylamide, N-benzoyl-DL-arginine-2-naphthylamide, 2-naphthyl phosphate (pH 5·4), naphthol-AS-BI-phosphate, 2-naphthyl--D-glucopyranoside, 1-naphthyl-N-acetyl--D-glucosaminide and 2-naphthyl--L-fucopyranoside, but the following substrates are not hydrolysed: 2-naphthyl myristate, N-glutaryl-phenylalanine-2-naphthylamide, naphthol-AS-BI--D-glucuronide, 6-bromo-2-naphthyl--D-glucopyranoside and 6-bromo-2-naphthyl--D-mannopyranoside. The fatty acid profile consists largely of 15 : 0 iso (46·4±2·2 %), 17 : 0 iso 3-OH (15·3±0·2 %) and summed feature 4 (15 : 0 iso 2-OH and/or 16 : 17c/t, 17·0±1·3 %). The G+C content of the DNA is 35·3±0·3 mol% (35·0 mol% for the type strain).
The type strain is DSM 14571T (=JCM 11413T=GTC 862T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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