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1 Cardiff School of Biosciences, Cardiff University, Main Building, Park Place, Cardiff CF10 3TL, UK
2 School of Earth, Ocean and Planetary Sciences, Cardiff University, Main Building, Park Place, Cardiff CF10 3YE, UK
Correspondence
John C. Fry
Fry{at}Cardiff.ac.uk
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Fluviicola taffensis RW262T is AF493694.
Micrographs of cells of strain RW262T and a table showing complete whole-cell fatty acid profiles of RW262T and the type species of other members of the family Cryomorphaceae are available as supplementary material in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Glöckner et al., 1999; Cottrell & Kirchman, 2000; O'Sullivan et al., 2002, 2004). However, the majority of the 16S rRNA gene sequences of members of ‘Bacteroidetes’ isolated from aquatic habitats are most closely related to those of uncultivated bacteria, indicating that a large amount of potentially interesting bacterial diversity has yet to be cultured (O'Sullivan et al., 2004). In the past few years there has been an increase in the descriptions of new genera of aquatic origin within the phylum ‘Bacteroidetes’, including Reichenbachia, Vitellibacter, Mesonia and Ulvibacter (Nedashkovskaya et al., 2003a, b, c, 2004, respectively), Belliella (Brettar et al., 2004), Gillisia (Van Trappen et al., 2004), Kordia (Sohn et al., 2004), Arcicella (Nikitin et al., 2004) and Formosa (Ivanova et al., 2004).
The novel family Cryomorphaceae has recently been described as containing four genera of marine origin: Brumimicrobium, Cryomorpha and Crocinitomix (Bowman et al., 2003), and Owenweeksia (Lau et al., 2005). According to 16S rRNA gene phylogeny, the family Cryomorphaceae branches between the families Flavobacteriaceae and Bacteroidaceae (Bowman et al., 2003). It also exhibits greatest phenotypic similarity to the well-defined family Flavobacteriaceae (Bernardet et al., 1996). On the basis of polyphasic taxonomic data and in adherence with the proposed minimal standards for describing new taxa of the closely related family Flavobacteriaceae (Bernardet et al., 2002), we describe a novel freshwater member of the family Cryomorphaceae, Fluviicola taffensis gen. nov., sp. nov.
Strain RW262T was isolated from water of the River Taff (Cardiff, UK; Ordnance Survey map reference SO 783 165) in January 2000, after 6 days incubation at 20 °C on CYT agar (1 g pancreatic digest of casein, 0·5 g CaCl2.2H2O, 0·5 g MgSO4.7H2O, 0·5 g yeast extract and 15 g purified agar, per litre distilled water; pH 7·2; Holmes, 1992). The strain was subsequently purified on Plate Count agar (PCA; Oxoid) and stored at –80 °C in liquid medium supplemented with 20 % (v/v) glycerol. Strain RW262T was selected for further investigation based on the results of 16S rRNA gene-targeted oligonucleotide hybridizations described in a previous study (O'Sullivan et al., 2004).
The following phenotypic tests were performed on strain RW262T and Crocinitomix catalasitica NCIMB 1418T as a reference. Unless otherwise stated, the strains were revived from freezer stocks at 20 °C on either nutrient agar (NA; Oxoid) or PCA prior to investigation. The agar used to grow Crocinitomix catalasitica was supplemented with artificial sea water (24·7 g NaCl, 0·7 g KCl, 6·3 g MgSO4.7H2O, 4·6 g MgCl2.6H2O, 1 g anhydrous CaCl2 and 0·2 g NaHCO3, per litre distilled water). Gram-testing was by the KOH method (Gregerson, 1978) and flexirubin pigments were determined according to Fautz & Reichenbach (1980). Growth on Tryptone Soya agar (TSA; Oxoid), Marine agar 2216 (MA2216; Difco), MacConkey agar and Cetrimide agar (Oxoid) was assessed after 1 week. Cell size and gliding motility of strain RW262T was established by phase-contrast microscopy of colonies after cultivation (3 days) under high humidity on agar. For scanning electron microscopy, RW262T cells were fixed (1 h, 3 % glutaraldehyde), washed (0·1 M cacodylate buffer, pH 7·5), post-fixed (1 % OsO4), dehydrated in ethanol, critical-point dried and coated with gold. Temperature and salinity requirements were determined by incubation on NA at 4, 16, 30 and 37 °C and with 0, 2·5, 5 and 10 % NaCl, respectively. Individual colony formation indicated positive results and growth without colony formation indicated weakly positive results. Standard methods (Smibert & Krieg, 1994) were used for oxygen requirements (thioglycollate medium), oxidase and catalase activity, DNA hydrolysis (DNASE agar), starch hydrolysis (NA plus 1 g starch l–1) and xylanase activity (NA plus 4 g birch wood xylan l–1). Nitrate and nitrite reduction, indole production, urease activity, and hydrolysis of Tween 80, gelatin and arginine were analysed according to Cowan & Steel (1975). Strains were also characterized using an API 20NE kit (bioMérieux), according to the manufacturer's instructions, except that the incubation was performed at 20 °C and Crocinitomix catalasitica was inoculated in artificial sea water containing 1 g Casamino acids l–1 and 1 ml trace elements l–1 (2·85 g H3BO3 l–1, 1·8 g MnCl2.4H2O l–1, 1·36 g FeSO4 l–1, 26·9 mg CuCl2.2H2O l–1, 20·8 mg ZnCl2 l–1, 40·4 mg CoCl2.6H2O l–1, 25·2 mg Na2MoO4.2H2O l–1 and 1·77 g sodium tartrate l–1). Antimicrobial susceptibility was assessed with antibiotic diffusion discs (Mast Diagnostics) with ampicillin (10 µg), kanamycin (30 µg), penicillin G (10 units), chloramphenicol (10 µg), streptomycin (10 µg), tetracycline (10 µg) and rifampicin (5 µg).
Fatty acid composition was determined with Crocinitomix catalasitica cultivated to confluence on MA2216, and strain RW262T cultivated on the equivalent of MA2216 but without NaCl (g l–1: 5 peptone, 1 yeast extract, 0·5 CaCl2.2H2O and 0·5 MgSO4.7H2O). Strains were grown at 20 °C for 72 h, harvested in PBS (Sigma) and freeze-dried. Fatty acid analyses followed the procedure described in the Microbial Identification System protocol (MIDI; http://www.midi-inc.com), and therefore represent the whole fatty acid composition of the cell hydrolysate. More-detailed analyses with other methods (Serrano-Carreon et al., 1992) showed no significant difference between hydrolysate fatty acid and phospholipid-derived fatty acid (PLFA) compositions, indicating that most fatty acids were derived from PLFAs.
The DNA base composition of strain RW262T was determined at the German Collection of Microorganisms and Cell Cultures (DSMZ; Braunschweig, Germany). DNA was isolated using a French pressure cell (Thermo Spectronic) and purified (Cashion et al., 1977). The G+C content was determined by HPLC (Mesbah et al., 1989). The 16S rRNA gene of strain RW262T was PCR amplified (O'Sullivan et al., 2004) from a small amount of purified colony biomass by using two sets of primers (27F, 1392R and 27F, 1492R; Lane, 1991). The PCR product obtained using primers 27F and 1392R was purified and sequenced (O'Sullivan et al., 2004), and the product obtained with primers 27F and 1492R was cloned by using the TOPO TA system (Invitrogen) and sequenced with primers M13F and M13R (O'Sullivan et al., 2002). A consensus from six overlapping sequences was compared with those most similar to RW262T in the GenBank database, including representative type strains from four families of the phylum ‘Bacteroidetes’. The CLUSTAL W alignment (Thompson et al., 1994) was trimmed to 1300 bp, evolutionary distances were calculated and a phylogenetic tree was constructed (O'Sullivan et al., 2004).
Strain RW262T was aerobic, Gram-negative, motile by gliding and flexirubin-pigmented. Cells were long flexible rods with rounded ends, 0·4–0·5 µm in diameter and 1·5–5·7 µm in length. Rarer longer filaments when observed were of up to 51 µm in length (see the supplementary figure in IJSEM Online). After 7 days on PCA at 20 °C, flat, transparent, shiny colonies, 1–5 mm in diameter, with a yellow–orange colour and creamy consistency, were produced. Growth occurred at 4 and 20 °C, but not in the presence of Na+ ions. Growth occurred on NA, PCA, TSA and DNASE agar, but not on MA2216, MacConkey agar or Cetrimide agar. The strain was catalase-positive, hydrolysed DNA and weakly hydrolysed gelatin. It was negative for nitrate and nitrite reduction; indole production; oxidase, 
-galactosidase, urease and xylanase activity; hydrolysis of agar, arginine, aesculin and starch; and acid production from carbohydrates. The strain could not utilize glucose, arabinose, mannose, mannitol, N-acetylglucosamine, maltose, gluconate, caprate, adipate, malate, citrate or phenyl acetate. It was resistant to chloramphenicol, streptomycin and kanamycin, but was susceptible to penicillin G, ampicillin, rifampicin and tetracycline.
The whole-cell fatty acid composition of strain RW262T is shown in Table 1 (taken from the supplementary table in IJSEM Online). The predominant cellular fatty acid was i15 : 0 (44·2 %). The G+C content of the genomic DNA of strain RW262T was 37·2 mol%. The phylogenetic position of strain RW262T was determined by analysis of the almost-complete 16S rRNA gene sequence. The greatest sequence similarity observed was with members of the families Cryomorphaceae and Flavobacteriaceae of the phylum ‘Bacteroidetes’. The 16S rRNA gene sequence of strain RW262T was 90 % similar to that of Ornithobacterium rhinotracheale LMG 9086T (GenBank accession no. ORU87101) and 89 % similar to that of Crocinitomix catalasitica NCIMB 1418T (GenBank accession no. AB078042) of the families Flavobacteriaceae and Cryomorphaceae, respectively. However, construction of a neighbour-joining phylogenetic tree clearly illustrated that strain RW262T formed a monophyletic lineage with the family Cryomorphaceae, positioned between the families Flavobacteriaceae and Bacteroidaceae (Fig. 1). The phylogenetic analysis indicated that strain RW262T represents a distinct genus within the Cryomorphaceae.
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). All members were also Gram-negative, catalase-positive, negative for indole production, and did not catalyse the hydrolysis of arginine, aesculin or starch. The 37·2 mol% G+C content of strain RW262T also fell within the 35–39 mol% known range for the family Cryomorphaceae (Bowman et al., 2003). The differential characteristics of strain RW262T and the type species of the four other Cryomorphaceae genera are shown in Table 2. Strain RW262T was only capable of weak growth at 4 °C, and was therefore not psychrotolerant as are other members of the family (Bowman et al., 2003). Strain RW262T was also capable of DNA hydrolysis, whereas other members were not. In addition, strain RW262T could be distinguished from Crocinitomix catalasitica NCIMB 1418T by its susceptibility to tetracycline and lack of growth at 30 °C, from Brumimicrobium glaciale IC156T by its aerobic metabolism and inability to reduce nitrate, from Cryomorpha ignava 1-22T by its gliding motility, and from Owenweeksia hongkongensis UST20020801T by its inability to grow at 37 °C or on 5 % NaCl and its lack of oxidase activity.
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). This suggests that RW262T may be a member of a freshwater clade within the family Cryomorphaceae which is distinct from the other marine members. Similar phylogenetic differentiation between freshwater and marine bacteria is commonplace within the closely related family Flavobacteriaceae, and was originally noted by Reichenbach et al. (1981). Specifically, the monophyletic branch representing the genus Flavobacterium contains mostly freshwater bacteria, whereas the monophyletic branch that represents many genera including Tenacibaculum, Polaribacter, Zobellia and Cellulophaga contains mostly marine bacteria.
The fatty acid profiles of strain RW262T and the type species of the four other Cryomorphaceae genera were examined (Table 1
). Cultivation conditions are known to influence fatty acid profiles (Männistö & Puhakka, 2001) and therefore conditions were standardized as much as possible to allow comparison with the results of Bowman et al. (2003). In this study, strain RW262T and Crocinitomix catalasitica were grown on MA2216 at 20 °C for 3 days (minus NaCl for RW262T), whereas in the study by Bowman et al. (2003) Crocinitomix catalasitica, B. glaciale and Cryomorpha ignava were grown on MA2216 at 10–12 °C for 3–5 days. Overall, the fatty acids identified for Crocinitomix catalasitica were very similar between the two studies; however, there were some differences in the proportions of individual fatty acids (Table 1). Like many flavobacteria and cryomorpha, strain RW262T contained high levels of C13–C17 branched-chain fatty acids (58·9 %), particularly saturated i15 : 0 (44·2 %) and unsaturated i15 : 1
10c (11·8 %) fatty acids. There was also a large proportion of hydroxy fatty acids (20·4 %), mainly composed of 3-OH i17 : 0 (12·3 %). The whole-cell fatty acid profiles shown in Table 1 clearly distinguish RW262T from the other members of the Cryomorphaceae.
The results of the polyphasic taxonomic analysis indicated that strain RW262T did not belong to any of the other genera currently described within the phylum ‘Bacteroidetes’. We therefore propose that strain RW262T should be classified as Fluviicola taffensis gen. nov., sp. nov.
Description of Fluviicola gen. nov.
Fluviicola [Flu.vi.i.co'la. L. masc. n. fluvius -ii river; L. suff. -cola (from L. masc. n. incola) inhabitant, dweller; N.L. masc. n. Fluviicola river dweller].
Non-flagellated, rod-shaped cells including rarer long filaments. Gram-negative. Strictly aerobic. Motile by gliding. Cell mass is pigmented yellow–orange and flexirubins are synthesized. Utilize carbohydrates for growth. Fatty acids contain a high proportion of branched-chain fatty acids (mainly i15 : 0 and i15 : 110c), as well as significant amounts of hydroxy fatty acids (mainly 3-OH i17 : 0). Isolated from freshwater environments, and do not grow in the presence of Na+ ions. 16S rRNA gene sequence analysis indicates that the genus is a member of the family Cryomorphaceae in the phylum ‘Bacteroidetes’. The type species is Fluviicola taffensis.
Description of Fluviicola taffensis sp. nov.
Fluviicola taffensis (taf.fen'sis. N.L. masc. adj. taffensis pertaining to the River Taff, a river in Wales).
Exhibits the following characteristics in addition to those properties described for the genus. Cells are 0·4–0·5 µm wide and 1·5–5·7 µm long, with rarer longer filaments of up to 51 µm in length. Colonies are 1–5 mm in diameter, circular, flat, transparent, shiny, yellow–orange and creamy on high nutrient solid media. Catalase-positive. Oxidase-negative. Growth occurs at 4–25 °C, with an optimum at about 20 °C. Growth occurs on NA, PCA, TSA and DNASE agar, but not on MA2216, MacConkey agar or Cetrimide agar. Negative for nitrate and nitrite reduction. Indole is not produced. Negative for -galactosidase, urease and xylanase activity. Capable of DNA hydrolysis and weak gelatin hydrolysis, but not hydrolysis of agar, arginine, aesculin or starch. Acid is not produced from glucose. Does not utilize glucose, arabinose, mannose, mannitol, N-acetylglucosamine, maltose, gluconate, caprate, adipate, malate, citrate or phenyl acetate. Resistant to chloramphenicol, streptomycin and kanamycin, but susceptible to penicillin G, ampicillin, rifampicin and tetracycline. The G+C content of the DNA is 37·2 mol%.
The type strain is RW262T (=NCIMB 13979T=DSM 16823T), which was isolated from water of the River Taff, Cardiff, UK.
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ACKNOWLEDGEMENTS |
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