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1 Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
2 Department of Food and Life Science, Sungkyunkwan University, Chunchun-dong 300, Jangan-gu, Suwon, Korea
3 National Research Laboratory of Molecular Ecosystematics, Institute of Probionic, Probionic Corporation, Bio-venture Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
Correspondence
Yong-Ha Park
yhpark{at}mail.kribb.re.kr
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9c as the major fatty acid. The polar lipid analysis indicated the presence of diphosphatidylglycerol, phosphatidylglycerol and phosphatidylethanolamine. The DNA G+C contents of strains YKJ-103T and YKJ-105 were 44 and 43 mol%, respectively. Strains YKJ-103T and YKJ-105 showed no difference in their 16S rDNA sequences, and their mean level of DNA–DNA relatedness was 92·3 %. Phylogenetic analysis based on 16S rDNA sequences showed that the two strains form a distinct phylogenetic lineage within the cluster comprising Psychrobacter species. Strains YKJ-103T and YKJ-105 exhibited 16S rDNA similarities of 96·6 % with the type strain of Psychrobacter proteolyticus, the closest Psychrobacter species, and of 94·5–95·9 % with type strains of other Psychrobacter species. On the basis of phenotypic properties, phylogenetic and genomic data, strains YKJ-103T and YKJ-105 should be placed in the genus Psychrobacter as members of a new species, for which the name Psychrobacter jeotgali sp. nov. is proposed. The type strain of the new species is strain YKJ-103T (=KCCM 41559T =JCM 11463T).
The GenBank accession numbers for the 16S rDNA sequences of strains YKJ-103T and YKJ-105 are AF441201 and AF441202, respectively.
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, 1986; Shaw & Latty, 1988; Juni, 1991; Bowman et al., 1996, 1997; Maruyama et al., 2000; Denner et al., 2001). These organisms had mainly been described as Moraxella-like, or included in the genera ‘Achromobacter’ or Acinetobacter (Juni, 1991). However, a group of psychrophilic coccobacilli with the above-mentioned properties, isolated from fish, processed meat and poultry products, was proposed as a new genus and new species, Psychrobacter immobilis (Juni & Heym, 1986). Subsequently, the family Moraxellaceae was proposed by Rossau et al. (1991) to accommodate the genera Moraxella and Acinetobacter as well as the genus Psychrobacter. At the time of writing, there were seven validly described Psychrobacter species: Psychrobacter frigidicola, Psychrobacter glacincola, P. immobilis, Psychrobacter pacificensis, Psychrobacter phenylpyruvicus, Psychrobacter proteolyticus and Psychrobacter urativorans. Subsequently, three more species in the genus Psychrobacter have been validly described: Psychrobacter faecalis (Kämpfer et al., 2002), Psychrobacter marincola and Psychrobacter submarinus (Romanenko et al., 2002). Two Gram-negative and moderately halophilic bacterial strains, YKJ-103T and YKJ-105, were isolated from the traditional Korean fermented seafood jeotgal, which is prepared with various kinds of seafood, seawater and other ingredients (Yoon et al., 2001). From the result of a preliminary taxonomic study, these organisms were considered to be related to the Psychrobacter–Moraxella group. Accordingly, the aim of the present study was to unravel the exact taxonomic positions of strains YKJ-103T and YKJ-105 by polyphasic characterization, including phenotypic properties, phylogeny based on 16S rDNA sequences and genomic relatedness. On the basis of the data presented here, strains YKJ-103T and YKJ-105 should be placed in the genus Psychrobacter as Psychrobacter jeotgali sp. nov. Strains YKJ-103T and YKJ-105 were isolated by dilution plating from jeotgal on marine agar 2216 (MA; Difco) at 30 °C. Cell biomass for isoprenoid quinone analysis and for DNA extraction was obtained from cultures in marine broth 2216 (MB; Difco) at 30 °C. The two strains were cultivated on a horizontal shaker at 150 r.p.m., and the cultures were checked for purity using a light microscope prior to harvesting by centrifugation. For fatty acid methyl ester (FAME) analysis, cell biomass of strains YKJ-103T and YKJ-105 was obtained after incubation for 6 days at 30 °C on MA.
Colony and cell morphologies were examined by using colonies grown on MA. Cell micromorphology was observed with a Nikon light microscope. The presence or absence of flagella was examined using transmission electron microscopy (TEM) with cells from an exponentially growing culture. For observation by TEM, cells were negatively stained with 1 % (w/v) phosphotungstic acid and the grids were examined after air drying by using a Philips CM-20 transmission electron microscope. Gram reaction was determined using a Gram Stain kit (bioMérieux) according to the manufacturer's instructions. Catalase, oxidase and urease activities, and hydrolysis of casein, gelatin, starch and Tween 80, were determined as described by Cowan & Steel (1965). Hydrolysis of aesculin and nitrate reduction were determined as described by Lanyi (1987). Hydrolysis of hypoxanthine, tyrosine and xanthine was performed on MA with substrate concentrations as described by Cowan & Steel (1965). Acid production from carbohydrates was determined as described by Leifson (1963). Enzyme activity was determined by using the API ZYM system; other physiological tests were performed with the API 20E system (both from bioMérieux). Utilization of various substrates for growth was determined as described by Yurkov et al. (1994). Requirements of yeast extract and vitamins for growth were determined in the liquid medium as used for the substrate utilization test, omitting yeast extract and vitamin B12 but supplementing with 0·1 % (w/v) acetate as the sole carbon and energy source. Yeast extract and vitamins were added to the medium at the following concentrations (l-1): yeast extract (0·005 g), p-aminobenzoic acid (1 mg), biotin (10 µg), thiamin hydrochloride (1 mg) and vitamin B12 (1 mg). Growth under anaerobic conditions was determined after incubation in an anaerobic chamber on anaerobically prepared MA. Growth at various NaCl concentrations was investigated on MA or in MB. Growth was measured on MA at 4–40 °C.
Chromosomal DNA was isolated and purified according to the method described previously (Yoon et al., 1996), except that ribonuclease T1 was used with ribonuclease A. Isoprenoid quinones were analysed as described by Komagata & Suzuki (1987) using reversed-phase HPLC. Polar lipids were extracted as described by Minnikin et al. (1984) and identified by two-dimensional TLC, followed by spraying with appropriate detection reagents (Komagata & Suzuki, 1987). For quantitative analysis of cellular fatty acid compositions, a loop of cell mass was harvested and FAMEs were prepared and identified according to the instructions of the Microbial Identification System (MIDI). The DNA G+C content was determined by the method of Tamaoka & Komagata (1984). DNA–DNA hybridization was performed fluorometrically by the method of Ezaki et al. (1989), using photobiotin-labelled DNA probes and microdilution wells.
16S rDNA was amplified by PCR using two universal primers as described previously (Yoon et al., 1998). The PCR product was purified by using a QIAquick PCR Purification kit (Qiagen). Purified 16S rDNA PCR product was sequenced using an ABI PRISM BigDye Terminator Cycle Sequencing Ready Reaction kit (Applied Biosystems) as recommended by the manufacturer. The purified sequencing reaction mixtures were electrophoresed using an Applied Biosystems 310 DNA sequencer. Alignment of sequences was carried out with CLUSTAL W software (Thompson et al., 1994). Gaps at the 5' and 3' ends of the alignment were omitted from further analysis. Phylogenetic trees were inferred by the neighbour-joining (Saitou & Nei, 1987), maximum-likelihood (Felsenstein, 1981) and maximum-parsimony (Kluge & Farris, 1969) methods in the PHYLIP package (Felsenstein, 1993). Evolutionary distance matrices for the neighbour-joining method were calculated with the algorithm of Jukes & Cantor (1969) in the DNADIST program. The stability of relationships was assessed by bootstrap analysis, based on 1000 resamplings of the neighbour-joining dataset, by using the SEQBOOT, DNADIST, NEIGHBOR and CONSENSE programs in the PHYLIP package.
Strains YKJ-103T and YKJ-105 were Gram-negative, non-spore-forming and non-motile bacteria. Their cells were cocci (diameter 1·1–1·6 µm) on MA. After 3–4 days incubation on MA, colonies of the two strains were smooth, glistening, low convex, circular to slightly irregular and cream in colour. Strains YKJ-103T and YKJ-105 grew optimally at 25–30 °C and grew at 4 and 36 °C but not above 37 °C. The two strains grew optimally at pH 6·0–7·5, and no growth was observed below pH 5·0. Strains YKJ-103T and YKJ-105 grew optimally in the presence of 2–3 % (w/v) NaCl; they grew in 0 and 9 % NaCl and weakly in the presence of 10 % NaCl but did not grow in the presence of more than 11 % NaCl. Strains YKJ-103T and YKJ-105 did not grow under anaerobic conditions on MA. The two strains required yeast extract for their growth in minimal salt medium. Strains YKJ-103T and YKJ-105 showed catalase, oxidase and urease activities. Tween 80 and tyrosine were hydrolysed, but no hydrolysis of aesculin, casein, gelatin, hypoxanthine, starch or xanthine was observed. The following enzymes were active in strains YKJ-103T and YKJ-105 when assayed with the API ZYM system: alkaline phosphatase, esterase (C4), lipase (C8), leucine arylamidase and cystine arylamidase. Naphthol-AS-BI-phosphohydrolase was weakly present in strain YKJ-103T but absent in strain YKJ-105. Nitrate was reduced to nitrite. Acetate, pyruvate, butyrate, succinate and ethanol were utilized as sole carbon and energy sources by the two strains. No acid was produced from the sugars used in this study. Phenotypic properties of strains YKJ-103T and YKJ-105 are summarized in Table 1, together with those of some Psychrobacter species.
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). The major fatty acid was C18 : 19c (Table 2). The cellular polar lipids found in strains YKJ-103T and YKJ-105 were diphosphatidylglycerol (DPG), phosphatidylglycerol (PG), phosphatidylethanolamine (PE) and some unidentified polar lipids. This polar lipid pattern was consistent with that of P. proteolyticus (Denner et al., 2001). The genomic DNA G+C contents of strains YKJ-103T and YKJ-105 were 44 and 43 mol%, respectively.
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). The relationship between this cluster (comprising strains YKJ-103T and YKJ-105 and Psychrobacter species) and the cluster comprising Moraxella species is supported by bootstrap analysis at a confidence level of 100 % (Fig. 1). The same tree topology was generated by the maximum-parsimony algorithm. In the maximum-likelihood tree, strains YKJ-103T and YKJ-105 formed an evolutionary lineage at the periphery of the phyletic radiation comprising Psychrobacter species. The levels of 16S rDNA similarity between strains YKJ-103T and YKJ-105 and the type strains of all Psychrobacter species that had been validly named at the time of writing ranged from 94·5 % (with P. phenylpyruvicus) to 96·6 % (with P. proteolyticus). Strains YKJ-103T and YKJ-105 showed levels of 16S rDNA similarity of 91·3–92·7 % with the type strains of those Moraxella species whose 16S rDNA sequences were available. Strains YKJ-103T and YKJ-105 exhibited two independent levels of DNA–DNA relatedness of 92·8 and 91·7 %.
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; Kodjo et al., 1997). There is a noteworthy difference in temperature for growth between these two genera (Bøvre, 1984; Kodjo et al., 1995, 1997; Bowman et al., 1997; Maruyama et al., 2000): most Psychrobacter species, including strains YKJ-103T and YKJ-105, grow optimally below 30 °C (Table 1
), whereas members of the genus Moraxella have an optimum growth temperature of 30–37 °C (Bøvre, 1984; Kodjo et al., 1995, 1997). Psychrobacter species grow at 4 °C, but Moraxella species do not. The phylogenetic analysis based on 16S rDNA sequences revealed that strains YKJ-103T and YKJ-105 are related more closely to the genus Psychrobacter than to the genus Moraxella (Fig. 1). In the phylogenetic tree based on 16S rDNA sequences, the two isolates occupy a distinct phylogenetic lineage within the cluster comprising Psychrobacter species (Fig. 1). This cluster joins with the phylogenetic clade comprising Moraxella species by a bootstrap value of 100 %. Chemotaxonomic analysis may be necessary to support the result of phylogenetic inference based on 16S rDNA sequences. However, there is little published chemotaxonomic data on the genus Psychrobacter. The cellular fatty acid analysis showed that strains YKJ-103T and YKJ-105 have similar profiles to Psychrobacter species (Bowman et al., 1996, 1997; Maruyama et al., 2000; Denner et al., 2001). C18 : 19c, which was the major fatty acid found in strains YKJ-103T and YKJ-105, is also the major component in Psychrobacter species, although some species simultaneously contain significant amounts of C16 : 17c (Bowman et al., 1996, 1997; Maruyama et al., 2000; Denner et al., 2001). P. pacificensis and P. proteolyticus have been reported to contain ubiquinone-8 (Q-8) as the predominant isoprenoid quinone (Maruyama et al., 2000; Denner et al., 2001). Accordingly, on the basis of the morphological and physiological data, phylogenetic inference and available chemotaxonomic data, strains YKJ-103T and YKJ-105 can be allocated to the genus Psychrobacter.
Strains YKJ-103T and YKJ-105 show almost identical phenotypic characteristics (Table 1). The two strains are also phylogenetically and genetically similar: there is no difference in the 16S rDNA sequences of the two strains (Fig. 1), and the mean genomic DNA relatedness between the two strains is 92·3 %, an appropriate level to place them in the same species (Wayne et al., 1987). The taxonomic position of strains YKJ-103T and YKJ-105 within the genus Psychrobacter is clear from the result of 16S rDNA sequence comparison with Psychrobacter species (Fig. 1). Levels of 16S rDNA similarity between strains YKJ-103T and YKJ-105 and Psychrobacter species are low enough to exclude the possibility of assigning the two strains to any previously described Psychrobacter species (Stackebrandt & Goebel, 1994). Accordingly, strains YKJ-103T and YKJ-105 can be considered as a new species of the genus Psychrobacter, even though DNA–DNA hybridization with Psychrobacter species was not performed. On the basis of these data, strains YKJ-103T and YKJ-105 should be placed within the genus Psychrobacter as a new species, for which the name Psychrobacter jeotgali sp. nov. is proposed.
Description of Psychrobacter jeotgali sp. nov.
Psychrobacter jeotgali (je.ot.ga'li. N.L. gen. n. jeotgali of jeotgal, traditional Korean fermented seafood).
Cells are cocci (diameter 1·1–1·6 µm) on MA. Gram-negative. Non-spore-forming. Non-motile. Colonies are cream in colour, smooth, glistening, low convex, irregular to slightly irregular. Aerobic. Growth occurs at 4 and 36 °C but not above 37 °C; optimum is 25–30 °C. Optimal pH for growth is 6·0–7·5; no growth is observed below pH 5·0. Grows in the presence of 0–10 % (w/v) NaCl; optimal NaCl concentration for growth is 2–3 % (w/v). Anaerobic growth does not occur on MA. Yeast extract is required for growth. Biotin, p-aminobenzoic acid, thiamin hydrochloride and vitamin B12 are not required for growth. Catalase-, oxidase- and urease-positive. Tween 80 and tyrosine are hydrolysed. Aesculin, casein, gelatin, hypoxanthine, starch and xanthine are not hydrolysed. Tryptophan deaminase activity is negative. When assayed with the API ZYM system, alkaline phosphatase, esterase (C4), lipase (C8), leucine arylamidase and cystine arylamidase are present but lipase (C14), valine arylamidase, trypsin, 
-chymotrypsin, acid phosphatase, -galactosidase, 
-galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase are not. Naphthol-AS-BI-phosphohydrolase is weakly present in strain YKJ-103T but absent in strain YKJ-105. Nitrate is reduced to nitrite. Acetate, pyruvate, butyrate, succinate and ethanol are utilized, but glucose, fructose, glutamate, citrate, lactate, formate, methanol and benzoate are not. Utilization of malate is variable. Acid is not produced from the following sugars: adonitol, L-arabinose, D-cellobiose, D-fructose, D-galactose, D-glucose, lactose, maltose, D-mannitol, D-mannose, D-melezitose, melibiose, myo-inositol, D-raffinose, L-rhamnose, D-ribose, D-sorbitol, stachyose, sucrose, D-trehalose or D-xylose. Predominant isoprenoid quinone is ubiquinone-8 (Q-8). Major fatty acid is C18 : 19c. Cellular polar lipids are diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and some unidentified polar lipids. DNA G+C content is 43–44 mol% (HPLC).
Isolated from the traditional Korean fermented seafood, jeotgal. Type strain is YKJ-103T, which has been deposited in the Korean Culture Center of Microorganisms as KCCM 41559T and in the Japan Collection of Microorganisms as JCM 11463T. Reference strain is YKJ-105.
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ACKNOWLEDGEMENTS |
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J.-H. Yoon, S.-J. Kang, S.-Y. Lee, and T.-K. Oh Loktanella maricola sp. nov., isolated from seawater of the East Sea in Korea Int J Syst Evol Microbiol, August 1, 2007; 57(8): 1799 - 1802. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S. E. Park, S.-J. Kang, and T.-K. Oh Rheinheimera aquimaris sp. nov., isolated from seawater of the East Sea in Korea Int J Syst Evol Microbiol, July 1, 2007; 57(7): 1386 - 1390. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, W. Kim, and T.-K. Oh Pigmentiphaga daeguensis sp. nov., isolated from wastewater of a dye works, and emended description of the genus Pigmentiphaga Int J Syst Evol Microbiol, June 1, 2007; 57(6): 1188 - 1191. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, S. Park, and T.-K. Oh Caenispirillum bisanense gen. nov., sp. nov., isolated from sludge of a dye works Int J Syst Evol Microbiol, June 1, 2007; 57(6): 1217 - 1221. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, S. Park, and T.-K. Oh Devosia insulae sp. nov., isolated from soil, and emended description of the genus Devosia Int J Syst Evol Microbiol, June 1, 2007; 57(6): 1310 - 1314. [Abstract] [Full Text] [PDF]
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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. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, J.-S. Lee, and T.-K. Oh Flavobacterium terrigena sp. nov., isolated from soil Int J Syst Evol Microbiol, May 1, 2007; 57(5): 947 - 950. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, S.-Y. Lee, and T.-K. Oh Phaeobacter daeponensis sp. nov., isolated from a tidal flat of the Yellow Sea in Korea Int J Syst Evol Microbiol, April 1, 2007; 57(4): 856 - 861. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-Y. Lee, S.-J. Kang, C.-H. Lee, and T.-K. Oh Pseudoruegeria aquimaris gen. nov., sp. nov., isolated from seawater of the East Sea in Korea Int J Syst Evol Microbiol, March 1, 2007; 57(3): 542 - 547. [Abstract] [Full Text] [PDF]
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Z. Aslam, J. H. Lim, W.-T. Im, M. Yasir, Y. R. Chung, and S.-T. Lee Salinicoccus jeotgali sp. nov., isolated from jeotgal, a traditional Korean fermented seafood Int J Syst Evol Microbiol, March 1, 2007; 57(3): 633 - 638. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, and T.-K. Oh Sulfitobacter marinus sp. nov., isolated from seawater of the East Sea in Korea Int J Syst Evol Microbiol, February 1, 2007; 57(2): 302 - 305. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, and T.-K. Oh Donghicola eburneus gen. nov., sp. nov., isolated from seawater of the East Sea in Korea Int J Syst Evol Microbiol, January 1, 2007; 57(1): 73 - 76. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, P. Schumann, S.-J. Kang, S.-Y. Jung, and T.-K. Oh Isoptericola dokdonensis sp. nov., isolated from soil Int J Syst Evol Microbiol, December 1, 2006; 56(12): 2893 - 2897. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, J.-S. Lee, and T.-K. Oh Brevundimonas terrae sp. nov., isolated from an alkaline soil in Korea Int J Syst Evol Microbiol, December 1, 2006; 56(12): 2915 - 2919. [Abstract] [Full Text] [PDF]
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S.-Y. Jung, H.-S. Kim, J. J. Song, S.-G. Lee, T.-K. Oh, and J.-H. Yoon Kribbia dieselivorans gen. nov., sp. nov., a novel member of the family Intrasporangiaceae. Int J Syst Evol Microbiol, October 1, 2006; 56(Pt 10): 2427 - 2432. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, M.-H. Lee, S.-J. Kang, S.-Y. Lee, and T.-K. Oh Sphingomonas dokdonensis sp. nov., isolated from soil. Int J Syst Evol Microbiol, September 1, 2006; 56(Pt 9): 2165 - 2169. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, and T.-K. Oh Polaribacter dokdonensis sp. nov., isolated from seawater Int J Syst Evol Microbiol, June 1, 2006; 56(6): 1251 - 1255. [Abstract] [Full Text] [PDF]
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