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Int J Syst Evol Microbiol 55 (2005), 133-138; DOI  10.1099/ijs.0.02931-0
© 2005 International Union of Microbiological Societies

Chryseobacterium daecheongense sp. nov., isolated from freshwater lake sediment

Kwang Kyu Kim1, Hee-Sung Bae2, Peter Schumann3 and Sung-Taik Lee1

1 Department of Biological Sciences, Korea Advanced Institute of Science and Technology, 373-1 Guseong, Yuseong, Daejeon, Republic of Korea
2 Department of Biological Sciences, 331 Life Sciences Building, Louisiana State University, Baton Rouge, LA 70803, USA
3 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, D-38124 Braunschweig, Germany

Correspondence
Sung-Taik Lee
e_stlee{at}kaist.ac.kr


   ABSTRACT
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A novel nitrate-reducing bacterium, CPW406T, was isolated from the sediment of a shallow, freshwater lake. The strain was a Gram-negative, non-motile, non-spore-forming rod, which formed yellow-pigmented colonies on nutrient agar and contained a polyamine pattern with sym-homospermidine as the major compound, MK-6 as the predominant menaquinone, 15 : 0 iso and 17 : 0 iso 3-OH as the major fatty acids and phosphatidylethanolamine and several unknown lipids in the polar lipid profile. The 16S rRNA gene sequence of strain CPW406T was found to be most similar to that of the type strain of Chryseobacterium defluvii (DSM 14219T; 97·9 % similarity). However, DNA–DNA relatedness data and its phenotypic properties showed that strain CPW406T could be distinguished from all known Chryseobacterium species and thus represented a novel species, for which the name Chryseobacterium daecheongense sp. nov. is proposed; the type strain is CPW406T (=DSM 15235T=KCTC 12088T).

Published online ahead of print on 20 August 2004 as DOI 10.1099/ijs.0.02931-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Chryseobacterium daecheongense CPW406T is AJ457206.


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The genus Chryseobacterium was first described by Vandamme et al. (1994)Go. At that time six former Flavobacterium species were reclassified in this genus, and at present the genus Chryseobacterium comprises nine recognized species: Chryseobacterium balustinum, Chryseobacterium gleum (type species), Chryseobacterium indologenes, Chryseobacterium indoltheticum, Chryseobacterium meningosepticum, Chryseobacterium scophthalmum, Chryseobacterium defluvii (Kämpfer et al., 2003Go), Chryseobacterium joostei (Hugo et al., 2003Go) and Chryseobacterium miricola (Li et al., 2003Go). ‘Chryseobacterium proteolyticum’ has been described but the name has not been validated (Yamaguchi & Yokoe, 2000Go).

During the characterization of organisms isolated from the sediment of the Lake Daecheong, Korea for application in a photoautotrophic waste water-treatment bioreactor, strain CPW406T was recovered, showing yellow-pigmented colonies on nutrient agar (Difco) at 30 °C. This isolate was subcultured on this medium at 28 °C for 48 h for further analyses. Only for the analysis of fatty acids was strain CPW406T cultivated on trypticase soy agar (TSA; BBL) at 28 °C for 24 h for direct comparison with reference strains.

The Gram reaction was performed as described by Gerhardt et al. (1994)Go. Cell morphology was observed under a phase-contrast microscope (1000x magnification; Nikon), with cells grown for 3 days on nutrient agar. For scanning electron microscopy, cell preparation was done according to Seviour et al. (1984)Go and a XL30SFEG electron microscope (Philips) was used. Flexirubin-type pigment was detected according to the method of Fautz & Reichenbach (1980)Go. Oxidase activity was tested using Bactident-Oxidase strips (Merck) and catalase activity was tested using 3 % H2O2. Physiological characterization was performed using the miniaturized assay method of Kämpfer et al. (1997)Go and additional tests were performed using API 20NE, API 20E and API ZYM galleries according to the instructions of the manufacturer (bioMérieux). Acid production tests from sugar were performed as described previously (Yamaguchi & Yokoe, 2000Go).

Chemotaxonomic analyses were performed according to previously described procedures: respiratory quinones (Tindall, 1990Go); polyamines (Busse & Auling, 1988Go; Busse et al., 1997Go); polar lipids (Ventosa et al., 1993Go); fatty acids (Klatte et al., 1994Go; Kämpfer & Kroppenstedt, 1996Go).

Extraction of genomic DNA, PCR-mediated amplification of the 16S rRNA gene and sequencing of the purified PCR product were carried out according to Rainey et al. (1996)Go. The 16S rRNA gene sequence was aligned with published sequences retrieved from EMBL using ae2 editor (Maidak et al., 1994Go). The phylogenetic tree was constructed on the basis of the neighbour-joining method (Saitou & Nei, 1987Go); distances were estimated by the method of Jukes & Cantor (1969)Go using TREECON for Windows version 1.3b (Van de Peer & De Wachter, 1994Go).

DNA base composition (G+C content) was determined by HPLC after hydrolysis as described by Tamaoka & Komagata (1984)Go, and non-methylated {lambda} DNA (Sigma) was used as standard. For DNA–DNA hybridization, DNA was isolated by chromatography on hydroxyapatite (Cashion et al., 1977Go) and hybridization was performed as described by De Ley et al. (1970)Go with modifications (Escara & Hutton, 1980Go; Huß et al., 1983Go) using a Gilford System model 2527-R thermoprogrammer and plotter. Renaturation rates were calculated using the TRANSFER.BAS program (Jahnke, 1992Go).

Strain CPW406T formed visible colonies (about 2 mm in diameter) on nutrient agar within 24 h at 28 °C. No growth was observed at 5 °C or at temperatures above 42 °C within 14 days. The colonies were yellowish, translucent and shiny with entire edges, becoming mucoid after 3 days incubation. Cells were Gram-negative, non-motile, non-spore-forming rods (0·4–0·5 by 0·8–2·0 µm). Physiological characteristics are summarized in Table 1Go and in the species description.


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  		Table 1. Characteristics that differentiate strain CPW406T from the type strains of existing Chryseobacterium species

Species: 1, C. daecheongense sp. nov. CPW406T; 2, C. balustinum LMG 8329T; 3, C. defluvii DSM 14219T; 4, C. gleum LMG 8334T; 5, C. indologenes LMG 8337T; 6, C. indoltheticum LMG 4025T; 7, C. joostei LMG 18212T; 8, C. meningosepticum LMG 12279T; 9, C. miricola DSM 14571T; 10, C. scophthalmum LMG 13028T. Data for reference species were taken from Yabuuchi et al. (1983)Go, Holmes et al. (1984)Go, Segers et al. (1993)Go, Mudarris et al. (1994)Go, Yamaguchi & Yokoe (2000)Go, Kämpfer et al. (2003)Go, Hugo et al. (2003)Go and Li et al. (2003)Go. Acid production from salicin and sucrose was negative for all strains tested; hydrolysis of aesculin, casein and gelatin was positive for all strains tested. +, Positive; (+), weakly positive; –, negative; ND, not determined.

 
The chemotaxonomic properties of strain CPW406T were consistent with its classification into the genus Chryseobacterium (Vandamme et al., 1994Go; Hamana & Matsuzaki, 1990Go, 1991Go). The only respiratory quinone was menaquinone MK-6. The polyamines were composed of sym-homospermidine [37·8 µmol (g dry wt)–1], spermine [1·2 µmol (g dry wt)–1], spermidine [0·4 µmol (g dry wt)–1] and trace amounts of 1,3-diaminopropane, cadaverine and putrescine. The polar lipids were composed of phosphatidylethanolamine and several unknown polar lipids including aminolipid, glycolipid, phospholipid and unknown lipids.

The fatty acids 15 : 0 iso (51·2 %), 17 : 0 iso 3-OH (15·7 %) and summed feature 4 (15 : 0 iso 2-OH and/or 16 : 1{omega}7c/t, 10·3 %) were predominant and the detailed fatty acid composition is shown in Table 2Go. However, strain CPW406T showed a similar fatty acid profile to that of C. defluvii, which has a relatively larger amount of 15 : 0 iso and 13 : 0 iso compared with all other Chryseobacterium species. Although strain CPW406T and C. defluvii had similar profiles, there were some differences in amounts of components between the two.


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  		Table 2. Cellular fatty acid profiles of strain CPW 406T and species of the genus Chryseobacterium

Species: 1, C. daecheongense sp. nov. CPW406T; 2, C. balustinum (n=1); 3, C. defluvii (n=1); 4, C. gleum (n=5); 5, C. indologenes (n=45); 6, C. indoltheticum (n=1); 7, C. joostei (n=11); 8, C. meningosepticum (n=1); 9, C. miricola (n=1); 10, C. scophthalmum (n=7). Data for reference species were taken from Mudarris et al. (1994)Go (C. balustinum, C. indoltheticum, C. meningosepticum and C. scophthalmum), Hugo et al. (1999Go, 2003)Go (C. gleum, C. indologenes and C. joostei) and Kämpfer et al. (2003)Go (C. defluvii). n, The number of strains used. Type strains were included for all species. Fatty acids are listed using standard abbreviations (no. carbon atoms : no. double bonds). Fatty acids that account for less than 1 % of the total fatty acids in all strains studied are not shown; therefore, the percentages do not total 100 %. Means±SD are given. tr, Trace (less than 1 %); ND, not detected; ECL, equivalent chain-length (i.e. the identity of the fatty acid is unknown).

 
Analysis of the almost-complete 16S rRNA gene sequence of strain CPW406T, consisting of 1446 nucleotides, indicated its membership of the genus Chryseobacterium, the intrageneric relatedness of which ranges from 92·8 to 99·1 % among the type strains of species. The 16S rRNA gene sequence of strain CPW406T showed the highest similarity (97·9 %) to the type strain of C. defluvii, DSM 14219T, but relatively low sequence similarities (92·9–96·2 %) were found with all other Chryseobacterium species. Also, strain CPW406T occupied a distinct position in the phylogenetic tree, clustering with only C. defluvii (Fig. 1Go); bootstrap values indicated that almost all the branches and branch clusters were supported by high statistical significance.



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  		Fig. 1. Dendrogram, obtained by using 16S rRNA gene sequences and distance matrix (neighbour-joining) analysis, showing the position of strain CPW406T among species of the genus Chryseobacterium. Species of some genera within the family Flavobacteriaceae were used to define the root. Numbers at branching points refer to bootstrap values (1000 resamplings, only values above 50 % shown). Bar, 2 substitutions per 100 nucleotide positions. C., Chryseobacterium; B., Bergeyella; R., Riemerella.

 
According to 16S rRNA gene sequence analysis and subsequent phylogenetic analysis, only the DNA–DNA hybridization test between strain CPW406T and C. defluvii was needed to define a novel species, because sequence similarities (<97 %) between strain CPW406T and all Chryseobacterium species except C. defluvii were below the level indicative of relatedness at the species level (Stackebrandt & Goebel, 1994Go). The DNA–DNA hybridization test resulted in a re-association value of 33·9 %, which confirmed that strain CPW406T belonged to a distinct genomic species (Wayne et al., 1987Go).

Based on the phenotypic and genotypic data, strain CPW406T merits recognition as a novel species within the genus Chryseobacterium, for which the name Chryseobacterium daecheongense sp. nov. is proposed.

Description of Chryseobacterium daecheongense sp. nov.
Chryseobacterium daecheongense (dae.che.ong.en'se. N.L. neut. adj. daecheongense referring to Lake Daecheong, from where the type strain was recovered).

Cells are non-motile, non-spore-forming rods (0·4–0·5 by 0·8–2·0 µm). Gram-negative, oxidase- and catalase-positive. Good growth is observed on R2A agar, TSA and nutrient agar at 28–37 °C, but not on MacConkey agar or {beta}-hydroxybutyrate. Colonies are yellowish, translucent and shiny with entire edges, becoming mucoid after 3 days incubation. A bright-yellow pigment (flexirubin-type) is produced on nutrient agar: it is non-diffusible, non-fluorescent and turns reddish-brown upon the addition of 20 % KOH. Menaquinone MK-6 is the predominant quinone and sym-homospermidine is the major polyamine. Phosphatidylethanolamine is the major polar lipid; several unknown polar lipids are also present. The fatty acid profile is composed largely of 15 : 0 iso (51·2 %), 17 : 0 iso 3-OH (15·7 %) and summed feature 4 (15 : 0 iso 2-OH and/or 16 : 1{omega}7c/t, 10·3 %). Indole and H2S are not produced. Nitrate is reduced, but nitrite is not reduced. Aesculin, casein, gelatin and starch are hydrolysed, but urea is not. Acid is produced from D-cellobiose, D-fructose, glycerol, raffinose, trehalose and D-xylose, but not from L-arabinose, ethanol, D-glucose, lactose, D-maltose, D-mannitol, sucrose or salicin. The following compounds are utilized as sole carbon sources: {alpha}-cyclodextrin, dextrin, gentiobiose, D-glucose, glycogen, D-maltose, D-mannose, sucrose, D-trehalose, turanose, Tween 40, acetate, {alpha}-ketobutyrate, formate, propionate, methyl pyruvate, mono-methyl succinate, {alpha}-ketovalerate, alaninamide, L-alanine, L-asparagine, L-aspartate, glycyl-L-aspartate, L-glutamate, glycyl-L-glutamate, L-alanyl-glycine, L-leucine, L-ornithine, L-phenylalanine, L-proline, L-serine, L-threonine and glycerol. The following carbon sources are not utilized: adonitol, L-arabinose, D-arabitol, cellobiose, D-fructose, L-fucose, i-erythritol, D-galactose, N-acetyl-D-galactosamine, N-acetyl-D-glucosamine, methyl {beta}-D-glucoside, m-inositol, D-lactose, lactulose, D-mannitol, D-melibiose, D-psicose, D-raffinose, L-rhamnose, D-sorbitol, Tween 80, xylitol, cis-aconitate, {alpha}-hydroxybutyrate, {beta}-hydroxybutyrate, {gamma}-hydroxybutyrate, citrate, D-galactonate lactone, D-galacturonate, D-gluconate, D-glucosaminate, D-glucuronate, {alpha}-ketoglutarate, itaconate, DL-lactate, malonate, p-hydroxyphenylacetate, quinate, D-saccharate, sebacate, succinamate, succinate, bromosuccinate, glucuronamide, D-alanine, DL-carnitine, L-histidine, hydroxy-L-proline, L-pyroglutamate, D-serine, {gamma}-aminobutyrate, urocanate, phenylethylamine, inosine, putrescine, thymidine, uridine, 2,3-butanediol, 2-aminoethanol, glucose 1-phosphate, glucose 6-phosphate and DL-{alpha}-glycerol phosphate. Results from API ZYM tests are given in Table 3Go. The G+C content of the DNA is 36·6 %.


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  		Table 3. API ZYM profiles of strain CPW406T and the type strains of existing Chryseobacterium species

Species: 1, C. daecheongense sp. nov. CPW406T; 2, C. balustinum LMG 8329T; 3, C. defluvii DSM 14219T; 4, C. gleum NCTC 11432T; 5, C. indologenes NCTC 10796T; 6, C. indoltheticum ATCC 27950T; 7, C. joostei LMG 18212T; 8, C. meningosepticum NCTC 10016T; 9, C. miricola DSM 14571T; 10, C. scophthalmum LMG 13028T. Data for reference species were taken from Hugo et al. (2003)Go, except for those for C. defluvii and C. miricola. All organisms showed positive reactions for 2-naphthyl phosphate, 2-naphthyl caprylate, L-leucyl-2-naphthylamide, L-valyl-2-naphthylamide, 2-naphthyl phosphate, naphthol-AS-BI-phosphate and 1-naphthyl-N-acetyl-{beta}D-glucosaminide, and showed negative reactions for 2-naphthyl myristate, naphthol-AS-BI-{beta}D-glucuronide and 6-br-2-naphthyl-{alpha}D-mannopyranoside. The intensity of the colour was measured on a scale from 0 to 5, and interpreted as negative when values were between 0 and 1 and positive when values were between 2 and 5 (Mudarris et al., 1994Go).

 
The type strain is CPW406T (=DSM 15235T=KCTC 12088T), isolated from the sediment of Lake Daecheong, Korea.


   ACKNOWLEDGEMENTS
 
We would like to thank Anna Frühling, Ina Kramer and Jolante Swiderski for their expert technical assistance during this study. This work was supported by the 21C Frontier Microbial Genomics and Applications Center Program, Ministry of Science & Technology (Grant MG02-0101-001-2-2-0).


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Chryseobacterium haifense sp. nov., a psychrotolerant bacterium isolated from raw milk
Int J Syst Evol Microbiol, October 1, 2007; 57(10): 2344 - 2348.
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 Int. J. Syst. Evol. Microbiol.Home page
Y. Zhou, J. Dong, X. Wang, X. Huang, K.-Y. Zhang, Y.-Q. Zhang, Y.-F. Guo, R. Lai, and W.-J. Li
Chryseobacterium flavum sp. nov., isolated from polluted soil
Int J Syst Evol Microbiol, August 1, 2007; 57(8): 1765 - 1769.
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 Int. J. Syst. Evol. Microbiol.Home page
U. Behrendt, A. Ulrich, C. Sproer, and P. Schumann
Chryseobacterium luteum sp. nov., associated with the phyllosphere of grasses
Int J Syst Evol Microbiol, August 1, 2007; 57(8): 1881 - 1885.
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 Int. J. Syst. Evol. Microbiol.Home page
J.-H. Yoon, S.-J. Kang, and T.-K. Oh
Chryseobacterium daeguense sp. nov., isolated from wastewater of a textile dye works
Int J Syst Evol Microbiol, June 1, 2007; 57(6): 1355 - 1359.
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 Int. J. Syst. Evol. Microbiol.Home page
Z.-X. Quan, K. K. Kim, M.-K. Kim, L. Jin, and S.-T. Lee
Chryseobacterium caeni sp. nov., isolated from bioreactor sludge
Int J Syst Evol Microbiol, January 1, 2007; 57(1): 141 - 145.
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 Int. J. Syst. Evol. Microbiol.Home page
H.-Y. Weon, B.-Y. Kim, S.-H. Yoo, S.-W. Kwon, Y.-H. Cho, S.-J. Go, and E. Stackebrandt
Chryseobacterium wanjuense sp. nov., isolated from greenhouse soil in Korea.
Int J Syst Evol Microbiol, July 1, 2006; 56(Pt 7): 1501 - 1504.
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 Int. J. Syst. Evol. Microbiol.Home page
V. Gallego, M. T. Garcia, and A. Ventosa
Chryseobacterium hispanicum sp. nov., isolated from the drinking water distribution system of Sevilla, Spain.
Int J Syst Evol Microbiol, July 1, 2006; 56(Pt 7): 1589 - 1592.
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 Int. J. Syst. Evol. Microbiol.Home page
H. de Beer, C. J. Hugo, P. J. Jooste, M. Vancanneyt, T. Coenye, and P. Vandamme
Chryseobacterium piscium sp. nov., isolated from fish of the South Atlantic Ocean off South Africa
Int J Syst Evol Microbiol, June 1, 2006; 56(6): 1317 - 1322.
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 Int. J. Syst. Evol. Microbiol.Home page
M. S. Park, S. R. Jung, K. H. Lee, M.-S. Lee, J. O. Do, S. B. Kim, and K. S. Bae
Chryseobacterium soldanellicola sp. nov. and Chryseobacterium taeanense sp. nov., isolated from roots of sand-dune plants
Int J Syst Evol Microbiol, February 1, 2006; 56(2): 433 - 438.
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L. A. O'Sullivan, J. Rinna, G. Humphreys, A. J. Weightman, and J. C. Fry
Culturable phylogenetic diversity of the phylum 'Bacteroidetes' from river epilithon and coastal water and description of novel members of the family Flavobacteriaceae: Epilithonimonas tenax gen. nov., sp. nov. and Persicivirga xylanidelens gen. nov., sp. nov.
Int J Syst Evol Microbiol, January 1, 2006; 56(1): 169 - 180.
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 Int. J. Syst. Evol. Microbiol.Home page
K. Shimomura, S. Kaji, and A. Hiraishi
Chryseobacterium shigense sp. nov., a yellow-pigmented, aerobic bacterium isolated from a lactic acid beverage
Int J Syst Evol Microbiol, September 1, 2005; 55(5): 1903 - 1906.
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 Int. J. Syst. Evol. Microbiol.Home page
H. de Beer, C. J. Hugo, P. J. Jooste, A. Willems, M. Vancanneyt, T. Coenye, and P. A. R. Vandamme
Chryseobacterium vrystaatense sp. nov., isolated from raw chicken in a chicken-processing plant
Int J Syst Evol Microbiol, September 1, 2005; 55(5): 2149 - 2153.
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