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Int J Syst Evol Microbiol 56 (2006), 2921-2925; DOI  10.1099/ijs.0.64564-0
© 2006 International Union of Microbiological Societies

Flavobacterium glaciei sp. nov., a novel psychrophilic bacterium isolated from the China No.1 glacier

De-Chao Zhang1,2, He-Xiang Wang2, Hong-Can Liu1, Xiu-Zhu Dong1 and Pei-Jin Zhou1

1 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100080, P. R. China
2 State Key Laboratory for Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing 100094, P. R. China

Correspondence
Pei-Jin Zhou
zhou{at}sun.im.ac.cn


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A novel psychrophilic, yellow-pigmented and obligate aerobic bacterium, strain 0499T, was isolated from the China No.1 glacier. Strain 0499T displayed the common phenotypic and chemotaxonomic features of the genus Flavobacterium, containing menaquinone-6 (MK-6) as the major quinone and C15 : 0, iso-C15 : 0, C17 : 1{omega}6c and summed feature 3 (C16 : 1{omega}7c/iso-C15 : 0 2-OH) as the major fatty acids. Optimal growth occurred at 21 °C. The genomic DNA G+C content was 36.5 mol%. Phylogenetic analysis based on 16S rRNA gene sequence similarity showed that strain 0499T was related to members of the genus Flavobacterium, sharing the highest sequence similarities with Flavobacterium succinicans (97.9 %), Flavobacterium granuli (97.4 %) and Flavobacterium hydatis (97.2 %). On the basis of phenotypic characteristics, phylogenetic analysis and DNA–DNA relatedness data, a novel species Flavobacterium glaciei is proposed with strain 0499T (=CGMCC 1.5380T=JCM 13953T) as the type strain.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Flavobacterium glaciei sp. nov. strain 0499T is DQ515962.

A table detailing the cellular fatty acid contents of Flavobacterium glaciei sp. nov. and related taxa is available as supplementary material in IJSEM Online.


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The genus Flavobacterium was proposed by Bergey et al. (1923)Go. Since then, the description of the genus has been emended several times (Bernardet et al., 1996Go). It currently accommodates Gram-negative, non-spore-forming, yellow-pigmented and rod-shaped bacteria that are usually motile by gliding, contain menaquinone 6 (MK-6) as the sole respiratory quinone and have a DNA G+C content in the range of 32–37 mol%. At the time of writing, the genus Flavobacterium comprises 37 recognized species (Aslam et al., 2005Go; Horn et al., 2005Go; Nogi et al., 2005Go; Van Trappen et al., 2005Go; Yi et al., 2005Go; Wang et al., 2006Go; Yoon et al., 2006Go). Members of the genus Flavobacterium have been isolated from a wide range of temperate habitats including diseased fish, freshwater and river sediments, seawater and marine sediments, soil and microbial mats. A number of cold-adapted Flavobacterium species have also been isolated from glaciers, sea ice and Antarctic lakes.

During a survey of psychrophilic organisms from the China No.1 glacier, located in Xinjiang Uygur Autonomous Region, north-west China, we isolated a novel psychrophilic bacterial strain. Physiological and biochemical features, cellular fatty acid content, phylogenetic analysis based on the 16S rRNA gene sequence and DNA–DNA hybridization data indicated that the new isolate represents a novel species in the genus Flavobacterium.

Strain 0499T was isolated from frozen soil collected from the China No.1 glacier using previously described media and methods (Zhu et al., 2003Go). The strain was routinely grown aerobically at 21 °C on PYG medium containing the following components (l–1): 5 g bacto peptone (Difco), 0.2 g yeast extract (Oxoid), 5 g glucose, 3 g beef extract (Oxoid), 0.5 g NaCl and 1.5 g MgSO4.7H2O (pH adjusted to 7.0). Flavobacterium succinicans DSM 4002T and Flavobacterium hydatis NBRC 14958T were obtained from DSMZ and NBRC, respectively. Flavobacterium granuli KCTC 12201T was kindly provided by Dr Sung-Taik Lee. These strains were cultivated as recommended (Bernardet et al., 1996Go; Aslam et al., 2005Go) and used as reference strains.

DNA was extracted and purified as described by Sambrook et al. (1989)Go. The gene encoding 16S rRNA was amplified by PCR with the forward primer 5'-AGAGTTTGATCCTGGCTCAG-3' and reverse primer 5'-AAGGAGGTGATCCAGCCGCA-3' (Liu et al., 2000Go). The PCR product was sequenced using the ABI BigDye 3.1 sequencing kit (Applied Biosystems) and an automated DNA sequencer (ABI3730; Applied Biosystems). BLASTn searches with the nearly complete (1424 bp) 16S rRNA gene sequence of strain 0499T performed in GenBank and EMBL revealed that the novel isolate shared high sequence similarity (~97.9 %) with members of the genus Flavobacterium. Phylogenetic trees were constructed using the neighbour-joining (Saitou & Nei, 1987Go) and maximum-parsimony algorithms with Kimura's two-parameter model (Kimura, 1980Go) implemented in MEGA version 3.0 (Kumar et al., 2004Go). The resultant tree topologies were evaluated by bootstrap analysis based on 1000 replicates. Phylogenetic analysis (Fig. 1Go) based on a consensus 1145 bp length of 16S rRNA gene sequences showed that strain 0499T grouped with members of the genus Flavobacterium and formed a distinct cluster with F. succinicans DSM 4002T (97.9 %), F. granuli KCTC 12201T (97.4 %) and F. hydatis NBRC 14958T (97.2 %). Very similar tree topologies were obtained using the two different algorithms.


Figure 1
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  		Fig. 1. Neighbour-joining tree based on 16S rRNA gene sequences showing the phylogenetic relationships of strain 0499T and related species. The tree was rooted with Leeuwenhoekiella marinoflava. Numbers at nodes represent the bootstrap values (% of 1000 resampled datasets) greater than 50 %. GenBank accession numbers are given in parentheses. Bar, 1 % sequence divergence.

 
Colony morphology was observed on PYG medium after incubation at 21 °C for 24–48 h. Cell morphology was examined under a light microscope (BH-2; Olympus) using bacteria grown under the same conditions. The temperature range for growth was determined with a TN3F temperature-gradient incubator (Advantec). The pH range for growth was determined in PYG medium adjusted to various pH values with HCl or NaOH (1 M l–1). Catalase, oxidase, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, lecithinase and tryptophan deaminase activities, the Voges–Proskauer and the Simmons' citrate tests and the utilization of various substrates as sole carbon and energy source were examined according to Dong & Cai (2001)Go. Acid production from carbohydrates was determined as described by Leifson (1963)Go. Anaerobic growth was investigated in PYG medium in an anaerobic test tube filled with nitrogen gas. The presence of gliding motility was determined as described by Zhu et al. (2003)Go. Congo red adsorption was tested by directly flooding some colonies on agar plates with 0.01 % aqueous Congo red solution. The detection of flexirubin-type pigments using 20 % (w/v) KOH was performed according to Reichenbach (1989)Go. Other physiological tests were conducted as described by Wang et al. (2006)Go. Cells of strain 0499T were rod-shaped, Gram-negative, non-flagellated and non-gliding. Colonies on PYG agar were yellow, smooth, circular and convex with entire margins. Strain 0499T was distinguished from its nearest phylogenetic relatives, F. succinicans, F. granuli and F. hydatis by the following phenotypic characteristics: (i) strain 0499T was an obligate aerobic and non-gliding bacterium, whereas both F. succinicans and F. hydatis were facultatively anaerobic and motile; (ii) strain 0499T grew weakly on agar at 25 °C, whereas the optimal growth temperature of its phylogenetic relatives was 25–30 °C; (iii) strain 0499T did not produce beta-galactosidase, contrary to its phylogenetic relatives. Other phenotypic features that differentiated strain 0499T from its phylogenetic relatives and from some other psychrophilic Flavobacterium species are given in the species description and Table 1Go.


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  		Table 1. Differential characteristics of Flavobacterium glaciei, close phylogenetic relatives and some psychrophilic Flavobacterium species

Taxa: 1. F. glaciei 0499T; 2. F. succinicans DSM 4002T (Bernardet et al., 1996Go); 3. F. granuli KCTC 12201T (Aslam et al., 2005Go); 4. F. hydatis NBRC 14958T (Bernardet et al., 1996Go); 5. Flavobacterium xinjiangense JCM 11314T (Zhu et al., 2003Go); 6. Flavobacterium omnivorum JCM 11313T (Zhu et al., 2003Go); 7. Flavobacterium gillisiae ACAM 601T (McCammon et al., 2000Go); 8. Flavobacterium tegetincola ACAM 602T (McCammon et al., 2000Go); 9. Flavobacterium gelidilacus LMG 21477T (Van Trappen et al., 2003Go); 10. Flavobacterium frigidimaris DSM 15937T (Nogi et al., 2005Go); 11. Flavobacterium antarcticum JCM 12383T (Yi et al., 2005Go). +, Positive; –, negative; (+) weakly positive; V, variable among strains; ND, no data available.

 
Respiratory quinones were extracted and purified according to Collins (1985)Go and were analysed by HPLC (Wu et al., 1989Go) using menaquinone 6 (MK-6) from F. granuli KCTC 12201T as a reference. Cellular fatty acids were determined from a culture grown in PYG at 21 °C for 3 days and were extracted, methylated and analysed using the standard MIDI (Microbial Identification) procedure (Sasser, 1990Go). Cells of strain 0499T contained menaquinone 6 (MK-6) as the major respiratory quinone. The predominant cellular fatty acids of strain 0499T were C15 : 0 (13.9 %), summed feature 3 (C16 : 1{omega}7c/iso-C15 : 0 2-OH, 10.0 %), C17 : 1{omega}6c (9.5 %), anteiso-C15 : 0 (8.3 %), iso-C15 : 0 (8.2 %), iso-C15 : 1 (6.2 %), iso-C15 : 0 3-OH (5.2 %) and C15 : 1{omega}6c (5.2 %). The fatty acid profile of strain 0499T resembled those of other Flavobacterium species (Bernardet et al., 1996Go). Strain 0499T also contained the unsaturated fatty acid C17 : 1{omega}8c (3.0 %) and the hydroxylated fatty acid C17 : 0 3-OH (1.4 %) that are not commonly found in other Flavobacterium species. Detailed fatty acid profiles for strain 0499T, its closest phylogenetic relatives and some other psychrophilic Flavobacterium species are available in Supplementary Table S1 in IJSEM Online.

The DNA G+C content of strain 0499T was determined using the thermal denaturation method (Sly et al., 1986Go). DNA–DNA hybridization experiments were performed at 65.6 °C using the liquid renaturation method (De Ley et al., 1970Go) as modified by Huß et al. (1983)Go. Both experiments were carried out using a DU800 spectrophotometer (Beckman). The DNA G+C content of strain 0499T was 36.5 mol%. DNA–DNA relatedness between strain 0499T and F. succinicans DSM 4002T, F. granuli KCTC 12201T and F. hydatis NBRC 14958T was 48.4 %, 44.1 % and 31.9 %, respectively.

Based on phenotypic, chemotaxonomic and molecular data, it is concluded that strain 0499T represents a novel species of the genus Flavobacterium, for which the name Flavobacterium glaciei sp. nov. is proposed.

Description of Flavobacterium glaciei sp. nov.
Flavobacterium glaciei (gla.ci'ei. L. gen. n. glaciei of ice, referring to the isolation source, the China No.1 glacier).

Cells are Gram-negative rods, non-flagellated and non-gliding, 0.45–0.55 µm wide and 2.7–6.3 µm long. Colonies are yellow, smooth, circular and convex with entire margins and do not absorb Congo red. Psychrophilic and obligately aerobic. Produce catalase and cytochrome oxidase. Growth occurs at 4–25 °C and pH 6.0–9.0, with optimum growth at 21 °C and approximately pH 6.5–7.5. Growth occurs in the presence of 0–1 % (w/v) NaCl. Nitrate is reduced. Cells do not contain flexirubin-type pigments. Arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, lecithinase and tryptophan deaminase activities are absent. Simmons' citrate and Voges–Proskauer tests are negative. Hydrolyses gelatin, casein, starch and aesculin, but not agar, alginate, carboxymethylcellulose, chitin, pectin, DNA or urea. Acid and gas are not produced from carbohydrates. The following substrates are utilized as sole carbon source: D-glucose, maltose, sucrose, D-trehalose, D-mannose, dextrin, proline, L-glutamic acid and glucose 1-phosphate. The following substrates are not utilized as sole carbon source: fructose, fucose, D-galactose, L-arabinose, D-cellobiose, L-rhamnose, lactose, raffinose, D-melibiose, D-sorbitol, turanose, xylitol, glycerol, inositol, erythritol, serine, threonine, alanine, histidine, leucine, aspartic acid, malonic acid, lactic acid, acetic acid, citric acid, pyruvate, succinate or uridine. Cells contain menaquinone 6 (MK-6). The cellular fatty acids are C15 : 0 (13.9 %), summed feature 3 (C16 : 1{omega}7c/iso-C15 : 0 2-OH, 10.0 %), C17 : 1{omega}6c (9.5 %), anteiso-C15 : 0 (8.3 %), iso-C15 : 0 (8.2 %), iso-C15 : 1 (6.2 %), iso-C15 : 0 3-OH (5.2 %), C15 : 1{omega}6c (5.2 %), iso-C17 : 0 3-OH (4.2 %), C17 : 1{omega}8c (3.0 %), iso-C16 : 0 3-OH (3.0 %), iso-C17 : 1{omega}9c (2.7 %), C16 : 0 (2.1 %), C15 : 0 3-OH (2.0 %), C16 : 0 3-OH (1.7 %), anteiso-C15 : 1 (1.4 %) and C17 : 0 3-OH (1.4 %). The G+C content of the DNA is 36.5 mol%.

The type strain, 0499T (=CGMCC 1.5380T=JCM 13953T) was isolated from the China No.1 glacier in the Xinjiang Uygur Autonomous Region.


   ACKNOWLEDGEMENTS
 
We are grateful to Dr Sung-Taik Lee for providing the type strain of Flavobacterium granuli. This work was supported by the National Basic Research Program of China (2004CB719601).


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