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Institute of Microbiology, Chinese Academy of Sciences, Beijing 100080, PR China
Correspondence
Peijin Zhou
zhou{at}sun.im.ac.cn
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7c (17·7 %) and C15 : 16c (12·7 %). Strain ZF-8T showed a strong ability to degrade organic macromolecules such as starch, CM-cellulose, pectin and chitin. Its DNA G+C content is 35·1 mol%, and the major fatty acids are C16 : 17c (18·2 %) and C15 : 0 (9·9 %). Phylogenetic analysis based on 16S rDNA sequences indicated that ZF-6T and ZF-8T belong to the genus Flavobacterium and represent two novel species. DNA–DNA hybridization also supported the status of the two new isolates. The names Flavobacterium xinjiangense sp. nov. (type strain, ZF-6T=AS 1.2749T=JCM 11314T) and Flavobacterium omnivorum sp. nov. (type strain, ZF-8T=AS 1.2747T=JCM 11313T) are proposed for the two new isolates.
The GenBank accession numbers of the 16S rDNA sequences of ZF-6T and ZF-8T are AF433173 and AF433174, respectively.
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). As 80 % of the biosphere has a temperature that remains permanently below 5 °C, cold-adapted micro-organisms are widely distributed in nature (Margesin & Schinner, 1994). Most of the psychrophiles that have been characterized so far originate from the Antarctic. Psychrophiles can also be found in permanently cold environments such as fresh and marine water, polar and high alpine soils and water, glaciers and frozen or chilled foodstuffs (Margesin & Schinner, 1994). The glacier is a relatively simple and closed ecosystem with a special biotic community, containing various psychrophilic and psychrotolerant organisms (Christner et al., 2000). In China, there are more than 46 000 glaciers, with a total area of >59 000 km2. China No. 1 glacier has an area of 1·74 km2 and is located in Xinjiang province, North-West China. Cold-adapted micro-organisms that inhabit these environments have not been well studied.
The genus Flavobacterium was proposed by Frankland in 1889 (Bergey et al., 1923); the description of the genus has been emended several times since then. Bernardet et al. (1996) proposed an emendment to the description, which states that the genus Flavobacterium represents predominantly gliding, pigmented bacteria and has menaquinone-6 as the primary respiratory quinone. Species of the genus Flavobacterium have DNA G+C contents of 32–37 mol%. Recently, several psychrophilic species of Flavobacterium have been reported (McCammon & Bowman, 2000; Humphry et al., 2001). In this study, we describe two newly isolated psychrophilic bacterial strains from the China No. 1 glacier. Morphological, physiological and chemotaxonomic studies indicated that the isolates should be placed in the genus Flavobacterium. Systematic studies on 16S rDNA similarity and DNA–DNA reassociation further distinguished the two isolates from known species in the genus Flavobacterium. The names Flavobacterium xinjiangense sp. nov. and Flavobacterium omnivorum sp. nov. are proposed for these isolates.
Samples of frozen soil from the China No. 1 glacier (Xinjiang province) were collected in September 1999. Samples were stored for 2 days in an ice chest until they could be processed in the laboratory. The frozen soil was suspended in an equal volume of liquid PYG medium and incubated for 1–2 days at 4 °C. Two millilitres of the suspension was used to inoculate PYG agar plates. The plates were incubated at 4 °C for 2 weeks. Strains ZF-6T and ZF-8T were obtained by selection of colonies that did not grow at 20 °C or above. PYG medium contained (l-1): 5·0 g polypeptone, 5·0 g tryptone, 10·0 g yeast extract, 10·0 g glucose and 40 ml salt solution. The salt solution, pH 7·2, contained (l-1): 0·2 g CaCl2, 0·4 g MgSO4.7H2O, 1·0 g K2HPO4, 1·0 g KH2PO4, 10·0 g NaHCO3 and 2·0 g NaCl. The reference strains, Flavobacterium gillisiae ACAM 601T, Flavobacterium xanthum ACAM 81T, Flavobacterium columnare ATCC 23463T and Flavobacterium frigidarium ATCC 700810T, were cultivated as recommended (Bernardet et al., 1996; McCammon & Bowman, 2000; Humphry et al., 2001). The size and morphology of cells grown in PYG medium at 11 °C for 16–24 h were measured and observed by transmission electron microscopy. Cells were negatively stained with 1 % (w/v) phosphotungstic acid; after air-drying, the grids were examined by using a model H-600 transmission electron microscope (Hitachi). Motility was determined by phase-contrast microscopy, using the hanging-drop technique (Skerman, 1967). For determination of gliding motility, strains were grown for 16–24 h at 11 °C on various dilute PYG media (solidified with 1·3 % agar, w/v), prepared as a thin layer on ethanol-rinsed microscope slides. Following incubation, the edges of the colonies were observed by using phase microscopy.
General physiological tests were performed as described by Smibert & Krieg (1981). Utilization of carbon and energy sources was investigated by the use of basal medium containing (l-1): 0·1 g yeast extract (Oxoid), 1 g (NH4)2HPO4 and 40 ml salt solution (pH 7·2). The medium was solidified with 1·3 % (w/v) purified agar (Oxoid). Carbon substrates were added at a concentration of 0·5 % (w/v). Testing for oxidative and fermentative acid production from carbohydrates was performed by using Leifson's medium (Leifson, 1963). Chitin hydrolysis was tested as described by Hsu & Lockwood (1975). The detection of flexirubin-type pigments using 20 % KOH and of extracellular glycans using the Congo red absorption test was performed according to McCammon & Bowman (2000). Growth temperature was determined using a TN3F temperature-gradient incubator (Advantec). For quantitative analysis of cellular fatty acids, a loop of cell mass grown on PYG agar at 11 °C for 2 days was harvested. Fatty acid methyl esters were prepared and identified using standard methods (Stackebrandt et al., 1995), and the results were compared to the database of fatty acids in the MIDI Sherlock Microbial Identification system (Microbial ID).
Genomic DNA was extracted and purified as described by Sambrook et al. (1989). The DNA G+C content was determined by the thermal denaturation method (Sly et al., 1986) with a Shimadzu UV-1206 spectrophotometer equipped with a TB-85 thermostat. DNA–DNA hybridization was carried out as described by Tindall et al. (1984). DNA fragments were labelled with [
-32P]dATP, following the instructions provided with the Nick Translation kit (Promega). The 16S rRNA genes of strains ZF-6T and ZF-8T were amplified by PCR using the Promega Taq kit with primers 43F and 1541R (Liu et al., 2000). Purified PCR products were ligated to the pGEM-T vector (Promega) and cloned according to the manufacturer's instructions. Sequencing reactions were carried out using the ABI PRISM BigDye Primer cycle sequencing kit, and sequencing was performed on an ABI 373S DNA sequencer (both Applied Biosystems). Almost-complete 16S rDNA nucleotide sequences of ZF-6T and ZF-8T were determined (1466 nt for both). The 16S rDNA sequences of ZF-6T and ZF-8T were aligned with reference sequences from GenBank by using the multiple sequence alignment program CLUSTAL W (Thompson et al., 1994). After removing non-base characters and ambiguous bases from the reference sequences, 1177 nt was used for DNA similarity calculation and phylogenetic tree construction. Evolutionary distance matrices were calculated by using the algorithm of Jukes & Cantor (1969) with the DNADIST program within the PHYLIP package (Felsenstein, 1993). A phylogenetic tree based on Knuc was constructed using the neighbour-joining method with the Kimura two-parameter model in TREECON for Windows (Van de Peer & De Wachter, 1994).
Cells of strains ZF-6T and ZF-8T were strictly aerobic, Gram-negative and rod-shaped with rounded ends (Fig. 1). Colonies on PYG agar were circular, convex with entire margins and a smooth appearance. The optimal temperature for growth was 11 °C; growth occurred at 0 °C, but not at 20 °C. Motility of the strains was not detected by phase-contrast microscopy in semi-solid medium culture. Gliding motility was not observed. The two strains were not able to grow on sea-water agar. Flexirubin pigments were absent. Colonies of ZF-6T on PYG medium were pale yellow, while those of ZF-8T were orange. The other characteristic physiological differences between ZF-6T and ZF-8T are summarized in Table 1.
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. The most abundant fatty acid of ZF-6T and ZF-8T was C16 : 17c, in line with other psychrophilic Flavobacterium species (Bernadet et al., 1996; McCammon & Bowman, 2000; Humphry et al., 2001). In addition, ZF-6T and ZF-8T did not seem to produce i-C17 : 17c, i-C17 : 15c or C17 : 0, which have commonly been found in the other psychrophilic Flavobacterium species (fatty acids representing <1 % were not considered). There were abundant monounsaturated and branched fatty acids in the membranes of ZF-6T and ZF-8T, which is consistent with other psychrophilic Flavobacterium species. Such fatty acids contribute to the maintenance of membrane fluidity at low temperature (Russell & Hamamoto, 1998).
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); they formed two distinct branches within the Flavobacterium clade, which were supported by bootstrap resampling values of 69 and 56 %, respectively.
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The high sequence similarity of the new isolates among themselves and to some other Flavobacterium species necessitated DNA–DNA hybridization tests. The genomic DNA of ZF-6T was 11·4, 19·3, 29·5 and 25·3 % similar to that of F. gillisiae ACAM 601T, F. xanthum ACAM 81T, F. frigidarium ATCC 700810Tand ZF-8T, respectively. The genomic DNA of ZF-8T was 7·9, 14·6, 21·6, 28·2 and 13·6 % similar to that of F. gillisiae ACAM 601T, F. xanthum ACAM 81T, F. columnare ATCC 23463T, F. frigidarium ATCC 700810Tand ZF-6T, respectively. Analysis of the results indicated that DNA similarities between ZF-6T, ZF-8T and other related Flavobacterium species were clearly below 70 % (which is considered to be the threshold value for the delineation of species).
On the basis of phenotypic, genotypic and phylogenetic data, it is clear that ZF-6T and ZF-8T are members of the genus Flavobacterium and represent two distinct and novel species, for which the names Flavobacterium xinjiangense sp. nov. and Flavobacterium omnivorum sp. nov. are proposed. The phenotypic characteristics that differentiate these species from other psychrophilic species in the genus Flavobacterium are given in Table 1
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Description of Flavobacterium xinjiangense sp. nov.
Flavobacterium xinjiangense (xin.jiang.en'se. N.L. neut. adj. xinjiangense pertaining to Xinjiang, an autonomous region in North-West China).
Gram-negative rods, 2·5–5 µm in length and 0·8 µm in width. Aerobic, psychrophilic, non-flagellated and non-gliding. Colonies are pale yellow, circular and smooth with entire edges. Optimal growth occurs at 11 °C; no growth occurs at 20 °C. No growth occurs in the presence of more than 3·5 % NaCl. Flexirubin pigments are not detected. Catalase- and oxidase-positive and strictly heteroorganotrophic. Metabolism is respiratory. H2S is produced. Nitrate is not reduced. No precipitate is produced on egg-yolk agar. The following biochemical tests are negative: arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase, ONPG hydrolysis, indole production, Voges–Proskauer reaction and Simmons' citrate test. Peptone and casamino acids, but not sodium nitrate, ammonium chloride or L-glutamate, serve as nitrogen sources. Does not produce any acid or gas from glucose, fructose, xylose, mannitol or maltose. Degrades casein, gelatin, aesculin and chitin, but not starch, Tween 80, agar, CM-cellulose, alginate, pectin, DNA, urea, uric acid or xanthine. The following are utilized as sole carbon sources: glucose, cellobiose, maltose, fructose, sucrose, arabinose and xylose. Sorbitol, sorbose, galactose, D-mannitol, raffinose, lactose, mannose, trehalose, glycerol, rhamnose, melibiose and inositol are not used as sole carbon sources. The major cellular fatty acids are C15 : 16c (12·7 %), i-C15 : 0 (11·6 %), C16 : 17c (17·7 %) and C17 : 16c (10·9 %). The G+C content of the DNA of the type strain is 34·4 mol%.
The type strain is ZF-6T (=AS 1.2749T=JCM 11314T), isolated from frozen soil from the China No. 1 glacier.
Description of Flavobacterium omnivorum sp. nov.
Flavobacterium omnivorum (om.ni.vor'um. L. n. omnis everything; L. v. vorare to devour; N.L. neut. adj. omnivorum eating everything, referring to the ability of the strain to degrade a wide range of macromolecules).
Gram-negative rods, 2–5 µm in length and 0·8 µm in width. Aerobic, psychrophilic, non-flagellated and non-gliding. Colonies are orange, circular and smooth with entire margins. Optimal growth occurs at 11 °C; no growth occurs at 20 °C. No growth occurs in the presence of more than 3·5 % NaCl. Flexirubin pigments are not detected. Catalase- and oxidase-positive and strictly heteroorganotrophic. Metabolism is respiratory. H2S is not produced. Nitrate is reduced to nitrite. ONPG is hydrolysed. No precipitate is produced on egg-yolk agar. The following biochemical tests are negative: arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase, indole production, Voges–Proskauer reaction and Simmons' citrate test. Peptone, casamino acids, sodium nitrate and ammonium chloride, but not L-glutamate, serve as nitrogen sources. Does not produce any acid or gas from glucose, fructose, xylose, mannitol or maltose. Degrades casein, aesculin, chitin, starch, alginate, CM-cellulose and pectin, but not gelatin, Tween 80, agar, DNA, urea, uric acid or xanthine. The following are utilized as sole carbon sources: glucose, cellobiose, maltose, fructose, sorbose, sucrose, lactose, rhamnose, mannose, trehalose, melibiose and arabinose. Sorbitol, galactose, D-mannitol, raffinose, glycerol, inositol and xylose are not used as sole carbon sources. The major cellular fatty acids are C15 : 0 (9·9 %), C16 : 17c (18·2 %) and i-C17 : 0 3-OH (9·4 %). The G+C content of the DNA of the type strain is 35·2 mol%.
The type strain is ZF-8T (=AS 1.2749T=JCM 11313T), isolated from frozen soil from the China No. 1 glacier.
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ACKNOWLEDGEMENTS |
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