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1 Department of Environmental Chemistry and Microbiology, National Environmental Research Institute, Frederiksborgvej 399, DK-4000 Roskilde, Denmark
2 Department of Ecology, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark
Correspondence
Niels Kroer
nk{at}dmu.dk
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Published online ahead of print on 17 October 2003 as DOI 10.1099/ijs.0.02398-0.
The GenBank accession numbers for the 16S rDNA sequences of strains D30T and D28 are respectively AF469612 and AF469613.
Detailed Biolog test results for the novel strains are available as supplementary material in IJSEM Online.
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; Giovannoni & Rappé, 2000). Members of the CFB group are widespread in the marine environment and are often associated with surfaces where they may benefit from their hydrolytic activity (Cottrell & Kirchman, 2000; Giovannoni & Rappé, 2000; Johansen et al., 1999; Suzuki et al., 2001). In addition to attached forms, the CFB group also includes pelagic (free-living) marine species (Giovannoni & Rappé, 2000; Gosink et al., 1998; Pinhassi et al., 1997).
The taxonomy of the CFB group has had a turbulent history since the proposal of the genus Cytophaga (Winogradsky, 1929). In recent years, studies on phylogenetic characterization have led to several reclassifications and emended descriptions of species within this group. Bernardet et al. (1996) presented a new description of the family Flavobacteriaceae and rearranged the taxonomy of the genus Flavobacterium. However, the generic relationship of members of the presumed [Flexibacter] maritimus rRNA branch was left open, which inspired a reclassification of several existing genera and descriptions of new genera, including Psychroserpens and Gelidibacter (Bowman et al., 1997), Psychroflexus (Bowman et al., 1998), Polaribacter (Gosink et al., 1998), Cellulophaga (Johansen et al., 1999; Bowman, 2000), Salegentibacter (McCammon & Bowman, 2000), Zobellia (Barbeyron et al., 2001) and Tenacibaculum. The latter genus contains the former [Flexibacter] maritimus, which has been reclassified to Tenacibaculum maritimum, the type species of the genus (Suzuki et al., 2001).
In the present study, two strains, D28 and D30T, related to the CFB group were isolated from a sea-water sample taken in the pelagic zone at 30 m depth in Skagerrak (57° 96' N 10° 78' E), Denmark. Skagerrak is a water body between Denmark and Norway that is strongly influenced by the North Atlantic Ocean. The strains were isolated on 10 %-strength ZoBell agar plates (ZoBell, 1946) from a 0·8 µm-filtered water sample (salinity 35 p.s.u., temperature 9 °C). Unless otherwise stated, full-strength ZoBell medium was used in all studies. The medium contained (l-1): 5·0 g Bacto peptone, 1·0 g yeast extract, 0·015 g FePO4.4H2O and 35 g sea salts (Sigma-Aldrich) l-1. For solidification of the medium, 1·5 % (w/w) agar was added.
Colony size, shape and colour were determined after 5 days incubation at 20 °C on ZoBell plates. Following acridine orange staining (Hobbie et al., 1977), photomicrographs of cells in exponential phase (overnight cultures incubated at 20 °C) and stationary phase (3 days incubation at 20 °C) were recorded with an Axiovert 100 TV microscope (Zeiss) fitted with an AT200 CCD camera. To test for gliding motility, the hanging drop method (Perry, 1973; Suzuki et al., 2001) was applied. Briefly, 20 µl drops of cell culture in full-strength and 1 % ZoBell medium were placed on microscope cover slips and potential gliding motility was examined at x1000 magnification. Lysis with 3 % KOH (Gregersen, 1978) was used to determine whether the isolates were Gram-positive or negative.
To study growth at different temperatures, overnight cultures were washed once (8200 g, 12 min, 10 °C) in ZoBell medium followed by streaking of 1 µl cell suspensions on ZoBell agar plates to obtain single colonies. The plates were incubated at 5, 10, 15, 20, 25, 30, 37, 40 and 45 °C for 9 days. To test the salt tolerance of the strains, ZoBell plates were prepared containing 0, 5, 10, 15, 20, 25, 30, 35, 40, 50 or 60 g sea salts l-1 or 35 g NaCl l-1. NaCl-containing plates were used to test whether micronutrients were required for growth. Growth at different pH values was studied on ZoBell plates in which pH was adjusted with HCl or NaOH to pH 4, 5, 6, 7, 8 and 9. Temperature resistance was tested by heating exponentially growing cells to 40, 50, 60, 70, 80, 90 and 100 °C for a maximum of 30 min, followed by streaking of subsamples on ZoBell plates. The plates were subsequently incubated at 30 °C for 7 days before the presence of colonies was examined.
Catalase activity was detected by the presence of bubbles after addition of one drop of 3 % H2O2 to colonies growing on solid ZoBell medium. Assays for cytochrome oxidase activity were considered positive when cells formed blue pigments after being streaked on filter paper wetted with 1 % N,N,N',N'-tetramethyl-p-phenyldiamine dihydrochloride (Barrow & Feltham, 1993). Flexirubin pigment was detected by colour shift when bacteria growing on solid ZoBell medium were exposed to a 20 % (w/v) KOH solution (Reichenbach, 1992). Growth on 0·4 % (w/v) DL-aspartate, L-leucine and sucrose was determined in a basal medium containing (l-1) 35 g sea salts (Sigma-Aldrich), 0·2 g NaNO3, 0·2 g NH4Cl and 0·05 g yeast extract according to Suzuki et al. (2001). Overnight cultures were washed three times in 1·5 % (w/v) sea salt solution and cells were inoculated to an OD590 of 0·1 in the growth medium. Bottles were incubated for 2 days at 20 °C and growth was followed spectrophotometrically. Growth in basal medium served as a control.
To test the ability of the strains to hydrolyse polymeric substrates, ZoBell plates were amended with 1 % (v/v) CM-chitin-RBV (Loewe Biochemica) or 1 % (w/v) of the following substrates: skimmed milk, starch and chromomeric azurine-cross-linked (AZCL) amylose, glucan, hydroxyethyl cellulose, curdlan, debranched arabinan, dextran, galactomannan, galactan, pullulan, xyloglucan, xylan, arabinoxylan, casein and collagen (all from Megazyme). Plates were incubated for 6 days at 30 °C and observed daily for colour reactions (AZCL substrates) or clearing zones (chitin, skimmed milk and starch) around colonies. Clearing zones on starch-amended media were detected after dripping Lugol solution (Fluka) on the surface of the plates.
Degradation of crystalline cellulose was tested by spotting 20 µl cell culture on Whatman 1 filter paper and lens-cleaning tissues placed on full-strength or 1 % ZoBell solid medium. Plates were incubated at 20 °C for 2 weeks and examined visually for dissolution of the cellulose by formation of translucent spots in the filter paper and lens-cleaning tissue. Growth on microcrystalline cellulose (Avicel; Merck) was tested in liquid basal medium containing 35 g sea salts and 0·67 g cellulose l-1. Bottles were incubated for 2 weeks at 30 °C and growth was followed spectrophotometrically.
Oxidation of 113 different carbon sources was determined using duplicate Biolog GN and triplicate GP plates as recommended by the supplier. Prior to Biolog characterization, overnight cultures were washed three times in 1·5 % (w/v) sea salts. Each well in the Biolog plates was inoculated with 150 µl cell suspension to an OD450 of 0·5, after which the plates were incubated at 30 °C. Development of purple colour in the wells, caused by reduction of tetrazolium dye, was detected with a 96-well plate reader at 590 nm.
The DNA base composition (mol% G+C) was analysed by the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ) by HPLC as described by Mesbah et al. (1989), Tamaoka & Komagata (1984) and Visuvanathan et al. (1989). Likewise, DNA–DNA hybridizations were performed by the DSMZ at 61 °C in 2xSSC (1xSSC is 0·15 M NaCl plus 15 mM sodium citrate) as described by De Ley et al. (1970), with the modifications described by Huß et al. (1983) and Escara & Hutton (1980). Approximately 95 % of the total 16S rDNA sequence of strain D30T was determined by the DSMZ by direct sequencing of PCR-amplified 16S rDNA. Genomic DNA extraction, PCR amplification of the 16S rDNA and purification of PCR products were carried out as described by Rainey et al. (1996). A partial 16S rDNA sequence for strain D28 was obtained by extracting DNA by boiling. DNA encoding 16S rRNA was amplified by PCR using primers F1 and R13 (Dorsch & Stackebrandt, 1992) and purified using the QIAquick PCR purification kit (Qiagen). A partial sequence of the 16S rDNA was obtained by sequencing the PCR product in both directions using primer F1 and a primer (5'-CGTATTACCGCGGCTGCT) modified after Lane et al. (1985). Sequences were aligned in BIOEDIT (Hall, 1999) against sequences from the Ribosomal Database Project II (Maidak et al., 2000). A phylogenetic tree was constructed by the neighbour-joining method (Jukes & Cantor, 1969) including Flexibacter flexilis as an outgroup. Ambiguous bases were excluded from the analysis. A tree and a bootstrap analysis with 500 sample replications were performed in TREECON for Windows (Van de Peer & De Wachter, 1994).
Strains D28 and D30T were both Gram-negative and did not produce flexirubin pigments. Colonies were convex, circular with spreading edges and bright yellow on ZoBell agar plates with 35 g sea salts l-1. After 5 days of incubation at 20 °C, colonies were 5–20 mm in diameter, depending on colony closeness. Exponentially growing cells were long and thread-like whereas stationary phase cultures were dominated by rods and spherical forms (not shown). Gliding motility was not observed.
Growth was observed at temperatures between 10 and 40 °C, while optimal growth occurred between 25 and 37 °C. At 40 °C, relatively few but large colonies appeared. No growth was detected at 50 °C and above; however, cells that had been exposed to 50 °C remained viable and grew well when returned to 30 °C. The strains grew well at pH 6–8, whereas no growth was observed after 6 days at pH 5. Relatively few but large colonies appeared at pH 9. No growth occurred at sea salt concentrations below 10 g l-1 (40 g sea salts l-1 equals 100 %-strength sea water). The strains grew well at sea-salt concentrations between 15 and 40 g l-1, while growth was slow at 50 g l-1 and very limited at 60 g l-1. No growth was observed on plates containing 35 g NaCl l-1, indicating that sea salts were required for growth.
Strains D28 and D30T both showed catalase and oxidase activity and their Biolog carbon respiration profiles were almost identical (details results available as supplementary material in IJSEM Online). Both strains utilized all the amino acids, except D-alanine, L-histidine, L-phenylalanine and D-serine, and grew on most of the polymers. Approximately one-third of the carbohydrates and carboxylic acids were utilized; however, D30T was capable of utilizing one more carbohydrate (D-melezitose), four more carboxylic acids (
-aminobutyric acid, D-glucosaminic acid, malonic acid, quinic acid) and one more polymer (mannan) than D28. Almost none of the D-isomers, except for 
-D-glucose (both strains) and D-melezitose and D-glucosaminic acid (strain D30T), supported growth, and none of the amino sugars, amines, glucosides, brominated compounds, alcohols or carbohydrates with an alcoholic group was used by any of the two strains.
The test of Suzuki et al. (2001) for the genus Tenacibaculum demonstrated growth of both strains on aspartate and sucrose in basal medium with 0·05 g yeast extract l-1, while weak growth was found on leucine (Fig. 1). The hydrolytic profiles of the strains were also identical, as they hydrolysed the same proteins (skimmed milk, AZCL casein and AZCL collagen) and showed positive reactions for glucose polymer -1,4-glucoside bonds (starch, AZCL -amylose and AZCL pullulan) and 
-1,4-glucoside bonds (AZCL hydroxyethyl cellulose, AZCL barley -glucan). None of the other tested substrates (CM-chitin-RBV, AZCL debranched arabinose, AZCL arabinoxylan, AZCL curdlan, AZCL dextran, AZCL galactan, AZCL galactomannan; AZCL xylan, AZCL xyloglucan) was hydrolysed by either strain. No degradation or growth on crystalline cellulose by D30T was observed.
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; Stackebrandt & Goebel, 1994). The similarity values between D30T and Tenacibaculum mesophilum MBIC 1140T and Tenacibaculum amylolyticum MBIC 4355T, on the other hand, were respectively 98·1 and 97·7 %. Thus, a DNA–DNA hybridization test was necessary to determine the relationship between D30T and these species (Schloter et al., 2000; Stackebrandt & Goebel, 1994). This showed that the DNA–DNA relatedness between D30T and T. mesophilum MBIC 1140T was 35·9 %, while that for T. amylolyticum MBIC 4355T was 34·3 %. Since the DNA relatedness values were well below the suggested 70 % limit for species identity (Wayne et al., 1987), we propose that D30T represents a novel species within the genus Tenacibaculum. The position of D30T among other members of the family Flavobactericeae is shown in Fig. 2.
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). Some differences were observed, however. The G+C content of strain D30T (35·2 mol%) was higher than those reported for any of the other Tenacibaculum species (30·3–32·5 mol%). In addition, unique characters of D28 and D30T were endocellulase activity, growth on sucrose, high salinity tolerance, formation of spherical cells in stationary phase, lack of Tween 80 metabolism and the formation of bright yellow colonies (Table 1).
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). T. mesophilum MBIC 1140T was isolated from a Japanese sponge homogenate, T. amylolyticum MBIC 4355T was isolated from Japanese macroalgae (Suzuki et al., 2001), T. maritimum NCIMB 2154T was isolated from a diseased red sea bream fingerling in Japan (Wakabayashi et al., 1986) and T. ovolyticum IAM 41318T was isolated from halibut eggs in Norway (Hansen et al., 1992). In contrast, strains D28 and D30T appeared to be free-living, as they were isolated from filtered (0·8 µm) sea water. However, they were capable of hydrolysing several polymeric compounds, as would be expected for surface-associated bacteria (Kirchman & Mitchell, 1982; Smith et al., 1992). Substantial release of bacteria from sinking particles to the surrounding water in pelagic marine environments has recently been demonstrated (Azam & Long, 2001; Riemann & Winding, 2001). Hence, prior to isolation, D28 and D30T could have been attached to particles. The closest phylogenetic relative of strains D28 and D30T is T. amylolyticum, characterized by starch hydrolysis. Strains D28 and D30T also hydrolysed starch but, in addition, they tested positive for endocellulase activity and growth on sucrose. Hence, they may be separated easily from the other Tenacibaculum species by these characters. The bright-yellow colour of the colonies may be used as a secondary unique characteristic.
Description of Tenacibaculum skagerrakense sp. nov.
Tenacibaculum skagerrakense (ska.ger.rak.en'se. N.L. neut. adj. skagerrakense of Skagerrak, Denmark, referring to the place of isolation).
Gram-negative, oxidase- and catalase-positive. Cells are rods (0·5x2–15 µm) during exponential growth. Spherical cells occur in stationary phase. Colonies are bright yellow and flexirubin-type pigment is absent. Requires at least 1/4-strength sea water for growth and grows in up to 150 %-strength sea water. Mesophilic: growth occurs at 10–40 °C, optimal growth around 25–37 °C and temperature resistance up to 50 °C. Grows at pH 6–9. Casein, collagen, hydroxyethyl cellulose, starch, barley -glucan and pullulan are hydrolysed. Growth occurs on sucrose and aspartate. Nitrate is reduced. G+C content of the DNA is 35·2 mol%.
The type strain is D30T (=ATCC BAA-458T=DSM 14836T). Isolated from the <0·8 µm fraction of a sea-water sample taken from Skagerrak, Denmark, at a depth of 30 m.
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ACKNOWLEDGEMENTS |
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D. H. Choi and B. C. Cho Lutibacter litoralis gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from tidal flat sediment. Int J Syst Evol Microbiol, April 1, 2006; 56(Pt 4): 771 - 776. [Abstract] [Full Text] [PDF]
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D. H. Choi, Y.-G. Kim, C. Y. Hwang, H. Yi, J. Chun, and B. C. Cho Tenacibaculum litoreum sp. nov., isolated from tidal flat sediment. Int J Syst Evol Microbiol, March 1, 2006; 56(Pt 3): 635 - 640. [Abstract] [Full Text] [PDF]
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H.-Y. Weon, B.-Y. Kim, S.-W. Kwon, I.-C. Park, I.-B. Cha, B. J. Tindall, E. Stackebrandt, H. G. Truper, and S.-J. Go Leadbetterella byssophila gen. nov., sp. nov., isolated from cotton-waste composts for the cultivation of oyster mushroom Int J Syst Evol Microbiol, November 1, 2005; 55(6): 2297 - 2302. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, and T.-K. Oh Tenacibaculum lutimaris sp. nov., isolated from a tidal flat in the Yellow Sea, Korea Int J Syst Evol Microbiol, March 1, 2005; 55(2): 793 - 798. [Abstract] [Full Text] [PDF]
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), aspartate (
) and leucine (
). Values were corrected for basal medium OD. Error bars represent ±1 SD (n=3). Strain D28 showed similar growth patterns.