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Taxonomy of Antarctic Flavobacterium Species: Description of Flavobacterium Gillisiae Sp

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Taxonomy of Antarctic Flavobacterium Species: Description of Flavobacterium Gillisiae Sp International Journal of Systematic and Evolutionary Microbiology (2000), 50, 1055–1063 Printed in Great Britain Taxonomy of Antarctic Flavobacterium species: description of Flavobacterium gillisiae sp. nov., Flavobacterium tegetincola sp. nov. and Flavobacterium xanthum sp. nov., nom. rev. and reclassification of [Flavobacterium] salegens as Salegentibacter salegens gen. nov., comb. nov. Sharee A. McCammon and John P. Bowman Author for correspondence: John P. Bowman. Tel: j61 3 6226 2776. Fax: j61 3 6226 2642. e-mail: john.bowman!utas.edu.au School of Agricultural 16S rRNA phylogenetic analysis of a number of yellow- and orange-pigmented Science, University of strains isolated from a variety of Antarctic habitats including sea ice, Tasmania, GPO Box 252-54, Hobart, Tasmania 7001, lakewater and cyanobacterial mats indicated a close relationship to the genus Australia Flavobacterium but distinct from known Flavobacterium species. Phenotypic properties, DNA GMC content and whole-cell fatty acid profiles of the Antarctic strains were consistent with those of the genus Flavobacterium. DNA–DNA hybridization analysis indicated the presence of two distinct and novel genospecies each isolated from a different Antarctic habitat. From polyphasic taxonomic data it is proposed that the two groups represent new species with the following proposed names: Flavobacterium gillisiae (ACAM 601T) and Flavobacterium tegetincola (ACAM 602T). In addition polyphasic analysis of the species ‘[Cytophaga] xantha’ (Inoue and Komagata 1976), isolated from Antarctic mud, indicated it was a distinct member of the genus Flavobacterium and was thus revived as Flavobacterium xanthum. Phylogenetic and fatty acid analyses also indicate that the species [Flavobacterium] salegens (Dobson et al. 1993), from Organic Lake, Antarctica, is misclassified at the genus level. It is proposed that this species belongs to a new genus, Salegentibacter salegens gen. nov., comb. nov. Keywords: Flavobacterium, Antarctica, sea ice, psychrophilic bacteria INTRODUCTION these problems resulting in Flavobacterium repre- senting predominantly gliding, pigmented bacteria The genus Flavobacterium is widespread in nature and which have a DNA GjC content of 32–37 mol% and has been isolated from many freshwater and soil menaquinone-6 as the primary respiratory quinone habitats. Several Flavobacterium species are pathogens (Bernardet et al., 1996). Phylogenetic analysis using of fish; however this genus appears primarily to play a 16S rRNA sequences and rRNA–DNA hybridization role in remineralization processes and exhibits strong experiments place Flavobacterium in the Flexibacter– macromolecular hydrolytic capabilities. Until recently Bacteroides–Flavobacterium phylum (Bauwens & De the nomenclatural status of the genus was hetero- Ley, 1981; Woese et al., 1990). Flavobacterium is the geneous and confused (Holmes et al., 1984; Bernardet type genus of the family Flavobacteriaceae which also et al., 1996). Recent studies have now resolved many of encompasses several other genera including Chryseo- ................................................................................................................................................. bacterium, Bergeyella, Riemerella, Ornithobacterium, The GenBank accession numbers for the 16S rRNA sequences of ACAM Empedobacter, Weeksella, Capnocytophaga, Myroides, strains 81T, 601T, 602T and 603 are AF030380, U85889, U85887 and U85888, Gelidibacter, Psychroserpens, Polaribacter, Psychro- respectively. flexus and various generically misclassified Cytophaga 01261 # 2000 IUMS 1055 S. A. McCammon and J. P. Bowman and Flexibacter species (Bernardet et al., 1996; Reichenbach, 1980). The detection of extracellular glucans Bowman et al., 1998). by the Congo red absorption test was performed by flooding plates with 0n01% (w\v) Congo red (McCurdy, 1969). The Several strains related to the genus Flavobacterium procedures of Hildebrand (1971) were followed to test for have been isolated from a number of Antarctic the degradation of pectin. CMC hydrolysis was tested by habitats. Inoue & Komagata (1976) isolated ‘[Cyto- overlaying nutrient agar with a thin layer of 0n5% (w\v) phaga] xantha’ from a mud pool near Syowa Station, CMC in tapwater agar and observing for hydrolysis zones Antarctica (68m S39m E). rRNA–DNA hybridization after 21 d incubation. experiments demonstrated this species was related to DNA base composition. Genomic DNA was extracted and Flavobacterium aquatile (Bernardet et al., 1996). Or- purified from cells using the Marmur & Doty (1962) ganic Lake, a shallow, meromictic, hypersaline water- procedure. The DNA GjC content was then determined body in the Vestfold Hills ice-free zone of Antarctica from thermal denaturation profiles using procedures de- (68m S78m E) has yielded the species [Flavobacterium] veloped by Sly et al. (1986). gondwanense and [Flavobacterium] salegens (Dobson DNA–DNA hybridization. The spectrophotometric renatur- et al., 1993). rRNA–DNA hybridization experiments ation rate kinetic procedure adapted by Huß et al. (1983) (Bernardet et al., 1996), fatty acids (Skerratt et al., was used to determine DNA–DNA reassociation values 1991; Bowman et al., 1998) and 16S rRNA sequence between genomic DNA of different strains. Genomic DNA analysis (Dobson et al., 1993) indicate that these was sheared to a mean size of 1 kb using sonication, di- species do not belong to the genus Flavobacterium but alysed overnight at 4 mCin2iSSC buffer (0n3 M NaCl, 0n03 M sodium citrate, pH 7n0), and adjusted in concen- instead represent phylogenetically distinct taxa within −" the Flavobacteriaceae.[Flavobacterium] gondwanense tration to approximately 75 µgml . Following denaturation has been subsequently renamed Psychroflexus gond- of the DNA samples, hybridization was performed at the wanensis (Bowman et al., 1998). Lactose-utilizing optimal temperature for renaturation (TOR) which was 25 mC below the DNA melting temperature and was calculated isolates from a highly oligotrophic freshwater lake in from the following equation: TOR mC l 48n5j(0n41imol% the Vestfold Hills were described as Flavobacterium GjC). The decline in absorbance over a 40 min interval of hibernum by McCammon et al. (1998). Finally a DNA mixtures and control DNA samples was used to number of yellow- and orange-pigmented isolates from calculate DNA hybridization values from the following sea ice and marine salinity lake samples (Franzmann et equation (Huß et al., 1983): al., 1990; Bowman et al., 1997a) have been found to be Percentage DNA hybridization phylogenetically related to the genus Flavobacterium; l (4AB A B 2 (A B)) 100% however 16S rRNA sequence data suggested these k k \ N i i strains represent potentially novel species. A and B represent the change in absorbance for two DNA samples being compared and AB represents the change in In this study phenotypic, fatty acid analysis and absorbance for equimolar mixtures of A and B. DNA genotypic data were utilized to ascertain the relation- hybridization values equal to or below 25% are considered ship of a number of Antarctic sea ice and lake isolates to represent background hybridization and are thus not to known Flavobacterium species. From this research it considered to be significant. was found the isolates represented two distinct and Fatty acid analysis. All strains were cultivated on trypticase novel species of Flavobacterium with the following soya agar (Difco) at 20 mC for 2 d, harvested and then proposed names: Flavobacterium gillisiae sp. nov. and lyophilized using a vacuum freeze-drier (Dynavac). Whole- Flavobacterium tegetincola.‘[Cytophaga] xantha’ was cell fatty acid profiles were quantitatively determined using also recognized as a distinct member of the genus gas chromatographic and GC-MS procedures (Nichols et Flavobacterium, and is revived as Flavobacterium al., 1986). The geometry and position of double bonds in xanthum. In addition the misclassified species [Flavo- monounsaturated fatty acids was confirmed using dimethyl- bacterium] salegens was elevated to genus status to disulfide derivatization and analysis using GC-MS. The reflect its distinct phylogenetic position and was double-bond positions are numbered from the methyl designated Salegentibacter salegens gen. nov., comb. (ω) end of the fatty acid. nov. Phylogenetic analysis. The 16S rRNA gene sequences for representatives of the isolates (ACAM 601T and ACAM 603T) were obtained in an earlier study (Bowman et al., METHODS 1997a). The sequence for ‘[Cytophaga] xantha’ ACAM 81T was obtained in this study. Conditions and reagents used for Strains and cultivation conditions. Protocols describing the isolation of the Antarctic strains investigated in this study PCR amplification and sequencing of 16S rRNA sequences were previously described (Bowman et al., 1997a). Isolates have been previously published (Bowman et al., 1997a). and reference strains investigated in this study are shown in Sequence reactions were prepared with the Prism Table 1. All strains utilized in the study were routinely dRhodamine terminator cycle sequencing ready reaction kit (Applied Biosystems). Electrophoresis and sequence reading cultivated on R2A medium (Oxoid) at 20 mC. were performed on a A377 DNA sequencer (Applied Bio- Phenotypic characterization. Most phenotypic tests have systems). The sequences used in the study were compared to been published previously (Bowman et al., 1997b). Flexi- the compilation of 16S rRNA genes available in the rubin pigments were detected by suspending cells
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