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1 Institute of Applied Biochemistry, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan
2 Research Institute of Biological Resources, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 6, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan
3 Science and Technology Promotion Foundation of Ibaraki, 2-1-6 Sengen, Tsukuba, Ibaraki 305-0047, Japan
Correspondence
Masatoshi Matsumura
aquacel{at}sakura.cc.tsukuba.ac.jp
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ABSTRACT |
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7cis, iso-C16 : 1, iso-C17 : 1, iso-C15 : 0 3-OH and iso-C16 : 0 3-OH. The DNA G+C content was 34·0–34·8 mol%. Phylogenetic analysis based on 16S rDNA sequences suggested that the strains belonged to the genus Flavobacterium and were closely related to Flavobacterium xanthum and Flavobacterium frigidarium, with sequence similarities of 96·9 and 96·3 %, respectively. In physiological and biochemical analyses, the isolates were differentiated from all known members of the genus Flavobacterium. The name Flavobacterium limicola is proposed for these novel strains, and the type strain is ST-82T (=JCM 11473T =DSM 15094T).
The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains ST-82T, ST-10 and ST-92 are AB075230, AB075231 and AB075232, respectively.
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TOPABSTRACTMAIN TEXTREFERENCES |
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). Several studies on molecular adaptation to cold conditions have increased interest in cold-adapted bacteria and exhibited the immense biotechnological potentials of, for example, the production of polyunsaturated fatty acids (Russell & Nichols, 1999) and the utilization of cold-active enzymes in specific biotransformations and environmental bioremediations (Margesin & Schinner, 1994; Feller et al., 1996; Russell, 1998).
Significant numbers of strains belonging to the genera Cytophaga and Flavobacterium in the Cytophaga–Flavobacterium–Bacteroides group have been found in various habitats, such as soils, sediments, fresh- and salt-water, cyanobacterial mats and the gills of diseased fish. These strains have been characterized by their adaptability to low temperatures (Bernardet et al., 1996; Bowman et al., 1997; Eilers et al., 2000). Several novel species belonging to the genus Flavobacterium and isolated from Antarctica have been described since 1998: Flavobacterium hibernum (McCammon et al., 1998), Flavobacterium gillisiae, Flavobacterium tegetincola (McCammon & Bowman, 2000) and Flavobacterium frigidarium (Humphry et al., 2001).
Recent molecular ecological studies using fluorescence in situ hybridization (FISH) and denaturing-gradient gel electrophoresis (DGGE) revealed that members of the Cytophaga–Flavobacterium group were abundant in cold marine sediments and freshwater ecosystems, and became dominant as a response to the input of organic substrates (Höfle, 1992; Llobet-Brossa et al., 1998; Rosselló-Mora et al., 1999; Ravenschlag et al., 2001). These findings suggest that members of the Cytophaga–Flavobacterium group play an important role in the primary decomposition of organic materials in cold environments. Indeed, many known species of the genera Cytophaga and Flavobacterium are capable of hydrolysing organic polymers, e.g. various proteins and polysaccharides (Bernardet & Grimont, 1989; Bernardet et al., 1996).
Three cold-adapted strains were newly isolated from cold freshwater sediments during our studies on the ecology of cold-adapted bacteria which contribute to the mineralization of complex organic materials. In this work, we show that the three novel cold-adapted isolates belong to the genus Flavobacterium and are clearly distinct from any other members of this genus, according to a polyphasic analysis based on physiological, chemotaxonomic and phylogenetic information.
Samples of freshwater sediments containing rich organic matters (ignition loss, 20 %; total carbon and nitrogen, 61·2 mg g-1; dry sediments, 5·3 mg g-1) were collected from the Shin River where it flows into Lake Kasumigaura in Ibaraki Prefecture (Japan). Strains ST-82T, ST-10 and ST-92 were isolated from the samples of diluted sediments using a PM medium containing (l-1): 1 g peptone, 0·5 g meat extract, 0·5 g NaCl and 10 ml sediment extracts prepared by autoclaving a mixture of 100 g sediments and 300 ml distilled water at 121 °C for 30 min. The medium was solidified with 1·5 % (w/v) agar and adjusted to pH 6·9. The incubation was performed at 4 °C for 1 month. Strains ST-82T, ST-10 and ST-92 were obtained in pure culture after three successive transfers to fresh agar medium.
Strains ST-82T, ST-10 and ST-92 all formed shiny, bright yellow, circular and convex colonies on trypticase soy agar (TSA; BBL). The cells were Gram-negative, ovoid to short rods, 1·1–3·2 µm long and 0·3–0·6 µm wide, and often had an elongated filament-like form (Fig. 1, top). Storage materials were not observed in the cells (Fig. 1, bottom). Neither spore formation nor motility by gliding was detected. Except for the lack of gliding motility, these morphological properties were typical of most of the species belonging to the genus Flavobacterium.
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. The optimum temperature for the growth of strains ST-82T (shown in Fig. 2) and ST-10 was 20 °C, whereas that of strain ST-92 was 15 °C. The doubling times of strains ST-82T, ST-10 and ST-92, grown at their optimum temperatures, were 5·7, 5·8 and 12·8 h, respectively. All strains were able to grow at 0 °C but none grew at 30 °C. The growth of the isolates was markedly inhibited at 25 °C: the doubling time at this temperature was approximately 5–7-fold that at the optimum temperature. Sodium chloride inhibited the growth of the isolates in either liquid or solid PY medium, although all isolates tolerated up to 1·5 % NaCl. The isolates were able to grow well on nutrient agar (Oxoid and Difco), TSA and R2A agar (Oxoid), but did not grow at all on sea-water agar.
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. These biochemical features were determined by standard methods (Fautz & Reichenbach, 1980; McCurdy, 1969; Smibert & Krieg, 1994) and API kits (API 20E, API 20NE and ID 32E, bioMérieux).
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-ketobutyric acid, -ketovaleric acid, propionic acid, starch, succinamic acid, alaninamide, L-alanine, L-alanylglycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl-L-aspartic acid, glycyl-L-glutamic acid, L-ornithine, L-proline, L-serine and L-threonine. Amino acid compounds were among the best substrates for the growth of the isolates. None of the isolates produced acid from any carbon source.
Hydrolysis of organic substrates was investigated on two-layer agar using one-tenth-strength PY medium. The hydrolysis reactions were determined by procedures described previously (Smibert & Krieg, 1994; Bowman et al., 1996; Humphry et al., 2001) except that agar degradation was determined by I/KI solution (Bowman, 2000). All three isolates were able to degrade casein, gelatin, starch, agar (no liquefaction), aesculin, tyrosine, urea and uric acid, but none were able to degrade ONPG, CM-cellulose, alginate, pectin, chitin, DNA, Tween 80, xylan or xanthine. In addition, the investigation of bacteriolytic ability using living and steamed cells of Escherichia coli NBRC 03301 and Pseudomonas putida NBRC 14164 was performed by the method of McCammon & Bowman (2000). Strains ST-82T, ST-10 and ST-92 degraded the steamed cells of both E. coli and P. putida, although they were unable to degrade the living cells of either bacterium.
Enzymic profiles of the isolates were tested using the API 20E, 20NE, ID32E and API ZYM galleries. All isolates possessed nearly identical profiles, showing positive activities for arginine dihydrolase, L-aspartic arylamidase, leucine arylamidase, valine arylamidase, cysteine arylamidase, alkaline and acid phosphatases, esterase, esterase-lipase, lipase, -glucosidase, N-acetyl-
-glucosamidase, -maltosidase, trypsin, chymotrypsin, urease and naphthol-AS-BI-phosphohydrolase (Table 2). The API ZYM enzymic profiles of the isolates closely resembled those of the other Flavobacterium species, as described by Bernardet et al. (1996) and Humphry et al. (2001).
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) at 5, 15 and 23 °C. All isolates produced more extracellular protease as the temperature was lowered to 5 °C: the relative protease activities (when the activity at 23 °C was defined as 1) per OD600 unit of strain ST-82T grown at 5 and 15 °C were 3·6 and 1·9, respectively. The activities of strains ST-10 and ST-92 were 2·3 and 1·5 at 15 °C, and 6·3 and 3·3 at 5 °C, respectively. Enhanced secretion at low temperatures seems to be a common feature of psychrophilic micro-organisms, and is advantageous for their adaptation to cold environments (Feller et al., 1996).
The G+C contents (Kamagata & Mikami, 1991) of the total DNA of strains ST-82T, ST-10 and ST-92 were 34·0, 34·8 and 34·6 mol%, respectively. All of the strains contained menaquinone-6 as the major respiratory quinone (Zhang et al., 2000). Fatty acid methyl ester analysis with a GC-MS system (Hanada et al., 2002) showed that the isolates had very similar whole-cell fatty acid profiles, including the following major constituents: C15 : 0, iso-C15 : 0, anteiso-C15 : 0, C15 : 1, iso-C15 : 1, C16 : 17cis, iso-C16 : 1, iso-C17 : 1, cyclo-C17 : 07,8cis, iso-C15 : 0 3-OH and iso-C16 : 0 3-OH (Table 3). For all three strains, the relative proportions of these components changed markedly according to the growth temperature (Table 3). At lower growth temperatures, C16 : 17cis increased while C15 : 0 and iso-C15 : 0 decreased. This drastic transition was observed between 23 and 15 °C in strains ST-82T and ST-10, and between 15 and 5 °C in strain ST-92.
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. The 16S rDNA sequence of strain ST-82T was very similar to those of strains ST-10 and ST-92, with sequence similarities of 99·9 and 99·0 %, respectively. Strains ST-10 and ST-92 also shared a high similarity, 99·1 %. The phylogenetic analysis, based on the neighbour-joining method (Saitou & Nei, 1987), showed that these isolates were placed as members of the genus Flavobacterium, and formed a distinct cluster with the Antarctic strains Flavobacterium xanthum, F. frigidarium and F. gillisiae in the tree (Fig. 3). The maximum-parsimony and maximum-likelihood trees, constructed by using the protocol of Kim et al. (2000), displayed almost the same branching pattern as the neighbour-joining tree (data not shown). Moreover, the maximum-likelihood tree supported the cluster of three isolates by a high bootstrap value of 98 %. The similarities in the 16S rDNA sequences between strain ST-82T and the closely related Antarctic species were as follows: F. xanthum, 96·9 %; F. frigidarium, 96·3 %; and F. gillisiae, 95·8 %.
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). The results are summarized in Table 4. The hybridization value of F. xanthum to the genomic probe of strain ST-82T was very low (4·2 %). Likewise, strains ST-82T, ST-10 and ST-92 showed low DNA–DNA hybridization (7·7–16·2 %) to the genomic probe of F. xanthum. These results clearly suggested that the three novel isolates were genotypically distinct from F. xanthum. The DNA–DNA hybridization values of ST-10 and ST-92 with the probe of ST-82T were greater than 70 %, which is the criterion of DNA relatedness for the definition of a species (Stackebrandt & Goebel, 1994).
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The physiological and biochemical features of the isolates were similar to those of the Antarctic strains F. xanthum, F. frigidarium and F. gillisiae. Particularly remarkable was the lack of gliding motility in these six strains, as gliding motility is typical for all other Flavobacterium species except Flavobacterium branchiophilum. However, the novel isolates were obviously differentiated from these three Antarctic strains by the following phenotypic characteristics: (1) the new isolates were freshwater species and were incapable of growth on marine 2216 agar or in the presence of 2·0 % NaCl (Fig. 2
), whereas the Antarctic strains were able to grow well on marine 2216 agar – in particular, F. frigidarium and F. gillisiae showed tolerance up to 5·0 and 9·0 % NaCl, respectively; (2) the isolates exhibited urease activity; (3) the isolates degraded agar; (4) the isolates hydrolysed tyrosine and formed brown diffusible pigments on tyrosine agar. In addition, the novel isolates were distinguished from the Antarctic species by the following features (summarized in Table 1): Congo red absorption; acid production from carbohydrates; hydrolysis of gelatin, starch, chitin, uric acid, xylan and Tween 80; production of cytochrome oxidase, arginine dihydrolase and H2S; and reduction of nitrate.
On the basis of the physiological, biochemical, chemotaxonomic and phylogenetic analyses, strains ST-82T, ST-10 and ST-92 were differentiated from any known species of the genus Flavobacterium and could be designated as a novel species within this genus, for which the name Flavobacterium limicola is proposed.
As strains ST-82T, ST-10 and ST-92 were able to adapt to low temperatures (for example, by the regulation of fatty acid composition for the maintenance of membrane fluidity at low temperatures), to degrade various organic polymers and bacterial cells of E. coli and P. putida, and to produce significant quantities of extracellular protease even at low temperatures, the isolates appear to play a role in the primary mineralization of complex organic materials in freshwater sediments during cold seasons. Recent molecular ecological studies revealed that members of the Cytophaga–Flavobacterium group have been found in large numbers in the natural environment, and that they became dominant as a response to the addition of organic substrates to cold marine sediments and freshwater systems (Höfle, 1992; Llobet-Brossa et al., 1998; Rosselló-Mora et al., 1999; Ravenschlag et al., 2001). Some species belonging to the Cytophaga–Flavobacterium group, including these newly identified isolates, can be considered as contributors to the primary mineralization of organic polymers in freshwater sediments.
Description of Flavobacterium limicola sp. nov.
Flavobacterium limicola (li.mi'co.la. L. n. limus mud; L. suff. n. -cola dweller; N.L. neut. n. limicola mud-dweller).
Cells are Gram-negative, ovoid to short rods, 1·1–3·2 µm long and 0·3–0·6 µm wide, occasionally with elongated filament-like forms. Non-sporulating, non-flagellated and non-gliding. Colonies on trypticase soy agar are circular and convex with bright yellow colour: flexirubin pigments are not detected. Congo red is absorbed. The temperature range for growth is 0–25 °C; no growth occurs at 30 °C. The optimum temperature for growth is 15–20 °C. Sodium chloride inhibits growth: tolerates up to 1·5 % NaCl. Grows well on nutrient agar and trypticase soy agar, but not on sea-water agar. Catalase and cytochrome oxidase are produced. Indole production, Voges–Proskauer and Simmons' citrate test are negative. Neither reduction of nitrate nor production of hydrogen sulfide occurs under any conditions. Lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase, -glucuronidase, -galactosidase and -galactosidase activities are absent. Arginine dihydrolase, L-aspartic arylamidase, leucine arylamidase, valine arylamidase, cysteine arylamidase, alkaline and acid phosphatases, esterase, esterase-lipase, lipase, -glucosidase, N-acetyl--glucosaminidase, -maltosidase, trypsin, chymotrypsin, urease and naphthol-AS-BI-phosphohydrolase are produced. -Glucosidase activity is detected by using aesculin as a substrate. Aerobic chemoheterotroph. No acid is produced from any carbohydrates. Amino acids such as L-alanine, L-alanylglycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl-L-aspartic acid, glycyl-L-glutamic acid, L-ornithine, L-proline, L-serine and L-threonine are better for growth than carbohydrates such as D-glucose, mannose, maltose, sucrose, starch, glycogen and dextrin. Yeast extract stimulates growth. Hydrolysis of some substrates is described in Table 1; in addition, urea and uric acid are hydrolysed, but not DNA, Tween 80, xylan or xanthine. Brown diffusible pigments are formed on tyrosine agar. No precipitation occurs on egg yolk agar. Steamed cells of E. coli and P. putida are lysed. Major respiratory quinone is menaquinone-6. Membrane lipids consist of a wide variety of branched, saturated, monounsaturated and 3-OH fatty acids; composition is dependent on growth temperature. DNA G+C content is 34·0–34·8 mol%.
The type strain ST-82T (=JCM 11473T =DSM 15094T) and the reference strains ST-10 (=JCM 11474 =DSM 14768) and ST-92 (=JCM 11475 =DSM 15093) were isolated from freshwater river sediments in Ibaraki Prefecture, Japan. The GenBank accession number for the 16S rDNA sequence of strain ST-82T is AB075230.
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ACKNOWLEDGEMENTS |
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K. A. Page, S. A. Connon, and S. J. Giovannoni Representative Freshwater Bacterioplankton Isolated from Crater Lake, Oregon Appl. Envir. Microbiol., November 1, 2004; 70(11): 6542 - 6550. [Abstract] [Full Text] [PDF]
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K. Mori, T. Kakegawa, Y. Higashi, K.-i. Nakamura, A. Maruyama, and S. Hanada Oceanithermus desulfurans sp. nov., a novel thermophilic, sulfur-reducing bacterium isolated from a sulfide chimney in Suiyo Seamount Int J Syst Evol Microbiol, September 1, 2004; 54(5): 1561 - 1566. [Abstract] [Full Text] [PDF]
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S. Van Trappen, I. Vandecandelaere, J. Mergaert, and J. Swings Flavobacterium degerlachei sp. nov., Flavobacterium frigoris sp. nov. and Flavobacterium micromati sp. nov., novel psychrophilic bacteria isolated from microbial mats in Antarctic lakes Int J Syst Evol Microbiol, January 1, 2004; 54(1): 85 - 92. [Abstract] [Full Text] [PDF]
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