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Laboratorium voor Microbiologie, Vakgroep Biochemie, Fysiologie en Microbiologie, Universiteit Gent, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium
Correspondence
Stefanie Van Trappen
stefanie.vantrappen{at}UGent.be
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ABSTRACT |
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6c, iso-C16 : 0, iso-C16 : 0 3-OH and summed feature 3 (which comprises iso-C15 : 0 2-OH, C16 : 17c or both) as major fatty acid components. On the basis of these results, three novel species are proposed, namely Flavobacterium degerlachei sp. nov. (consisting of 14 strains, with LMG 21915T=DSM 15718T as the type strain), Flavobacterium micromati sp. nov. (consisting of three strains, with LMG 21919T=CIP 108161T as the type strain) and Flavobacterium frigoris sp. nov. (consisting of 19 strains, with LMG 21922T=DSM 15719T as the type strain).
Published online ahead of print on 18 July 2003 as DOI 10.1099/ijs.0.02857-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains LMG 21915T, LMG 21922T, LMG 21919T, LMG 21471 and LMG 21474 are respectively AJ557886, AJ557887, AJ557888, AJ440988 and AJ441005.
A full tree showing the position of the three novel species within the genus Flavobacterium and a fuller table showing phenotypic characteristics are available as supplementary material in IJSEM Online.
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). Flavobacterium species have been isolated from diverse habitats such as fresh- and salt-water, soil, sediment, sea ice, diseased fish and microbial mats. Members of the CFB branch are highly abundant in freshwater and marine ecosystems and became dominant in response to the input of organic substrates (Höfle, 1992; Rosselló-Mora et al., 1999). These findings suggest that these bacteria may have a specialized role in the uptake and degradation of organic matter in cold, aquatic environments (Kirchman, 2002). Indeed, many species of the genus Flavobacterium are capable of the hydrolysis of organic polymers such as complex polysaccharides (Bernardet et al., 1996).
Several novel species that have been added to the genus Flavobacterium since 1996 originated from Antarctic habitats, e.g. Flavobacterium hibernum (McCammon et al., 1998), Flavobacterium gillisiae (McCammon & Bowman, 2000) and Flavobacterium frigidarium (Humphry et al., 2001), but only two species have so far been isolated from cyanobacterial mats: Flavobacterium tegetincola (McCammon & Bowman, 2000) and Flavobacterium gelidilacus (Van Trappen et al., 2003), which were collected from Antarctic lakes. Recently, three novel psychrophilic Flavobacterium species have been described: Flavobacterium limicola from freshwater sediments (Tamaki et al., 2003) and Flavobacterium xinjiangense and Flavobacterium omnivorum from the China No. 1 glacier (Zhu et al., 2003).
During the MICROMAT project (November 1998–February 2001), 746 bacterial strains were isolated under heterotrophic conditions from microbial mat samples that were collected from 10 Antarctic lakes in the Vestfold Hills (Lakes Ace, Druzhby, Grace, Highway, Pendant, Organic and Watts), the Larsemann Hills (Lake Reid) and the McMurdo Dry Valleys (Lakes Hoare and Fryxell) (Van Trappen et al., 2002). Salinity of these lakes ranges from fresh (Druzhby, Grace, Watts and Hoare) over hyposaline/saline (Ace, Highway, Pendant, Fryxell and Reid) to hypersaline (Organic). Numerical analysis of the fatty acid composition of the isolates revealed 41 clusters and 16S rRNA gene sequence analysis, performed on representative strains, showed that they belonged to the 
-, 
- and 
-subclasses of the Proteobacteria, the high and low-percentage G+C Gram-positives and the CFB branch (Van Trappen et al., 2002). Results of fatty acid and 16S rRNA gene sequence analyses showed that the diversity of heterotrophic bacteria in microbial mats from Antarctic lakes is very high. Moreover, many fatty acid clusters were shown to contain multiple taxa when tested by repetitive extragenic palindromic DNA (rep)-PCR fingerprinting, a technique that was used to investigate the genomic diversity of each fatty acid cluster more in detail (Van Trappen et al., 2001). Twenty-two isolates from fatty acid cluster 10 have already been described as a novel species, F. gelidilacus (Van Trappen et al., 2003).
In the present work, we have studied the taxonomic relationships of 36 strains from fatty acid clusters 5 and 6 (as delineated by Van Trappen et al., 2002) that are related to the genus Flavobacterium by polyphasic taxonomic characterization.
The isolates investigated are listed in Table 1. Strains were cultivated routinely on R2A medium (Difco) at 20 °C for 48 h or longer (LMG 21919T) or [for strains LMG 4031T (Flavobacterium pectinovorum) and LMG 8384T (Flavobacterium saccharophilum)] on TSA medium (BBL) at 20 °C for 48 h, except when mentioned otherwise.
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and rep-PCR fingerprinting (based on primers that targeted the repetitive extragenic palindromic sequence) was performed on all strains of fatty acid clusters 5 (75 strains) and 6 (five strains) of Van Trappen et al. (2002) using the primer GTG5 (Versalovic et al., 1991), as described by Rademaker & de Bruijn (1997) and Rademaker et al. (2000). Thirty-six of these strains, listed in Table 1
, could be divided into four different clusters according to their profile type (data not shown) and numerical analysis was carried out by using the Bionumerics software package (Applied Maths; available at http://www.applied-maths.com/), as described by the same authors. These clusters are hereafter referred to as rep-PCR profile types I (which comprises 14 strains), II (with three strains), III (with eight strains) and IV (with 11 strains). Versalovic et al. (1994) have shown that strains with the same rep-PCR profile are always closely related and this has been confirmed by several authors (e.g. Rademaker & de Bruijn, 1997).
Small-scale DNA extracts were prepared by using the method of Pitcher et al. (1989) and the almost-complete 16S rRNA gene sequences (1457–1480 nt) of strains LMG 21915T, LMG 21474, LMG 21919T, LMG 21922T and LMG 21471 were amplified by PCR with conserved primers (Coenye et al., 1999). PCR products were purified by using a QIAquick PCR Purification kit (Qiagen) according to the instructions of the manufacturer. Sequence analysis was performed by using an ABI Prism 3100 automatic DNA sequencer (Applied Biosystems), applying a BigDye Terminator Cycle Sequencing Ready Reaction kit (version 2.0; PerkinElmer Applied Biosystems), following the protocols of the manufacturer. Sequence assembly was performed by using the program AutoAssembler 1.4.0 (PerkinElmer Applied Biosystems). The most closely related sequences were found by using the FASTA program; sequences from reference strains were aligned and editing of the alignment and reformatting were performed with the BIOEDIT program (Hall, 1999) and ForCon (Raes & Van de Peer, 1999). Evolutionary distances were calculated by using the Jukes–Cantor evolutionary model and a phylogenetic tree (shown in Fig. 1) was constructed by using the neighbour-joining method (Saitou & Nei, 1987) with the TREECON program (Van de Peer & De Wachter, 1994). A full tree showing the position of the three novel species within the genus Flavobacterium is available as supplementary material in IJSEM Online. Dendrograms obtained by maximum-parsimony and maximum-likelihood analyses showed essentially the same topography (data not shown).
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The 16S rRNA gene sequences of the two representative strains of rep-PCR profile type I (LMG 21915T and LMG 21474) were almost identical (99·9 % sequence similarity) and showed 98·5 % similarity to F. gillisiae, 97·7 % to F. xinjiangense, 97·5 % to F. limicola, 96·9 % to F. omnivorum and 96·8 % to F. xanthum. The sequence of strain LMG 21919T, which belongs to rep-PCR profile type II, showed 97·4 % similarity to F. saccharophilum, 97·4 % to F. pectinovorum, 97·2 % to F. limicola and 96·9 % to F. omnivorum. The 16S rRNA gene sequences of the two representative strains of rep-PCR profile types III and IV (LMG 21922T and LMG 21471, respectively) show 99·1 % sequence similarity to each other and 98·4 % to F. gillisiae, 97·4 % to F. xinjiangense, 97·3 % to F. xanthum, 97·2 % to F. omnivorum and 97·1 % to F. limicola. Strains LMG 21922T and LMG 21915T showed 98·7 % sequence similarity to each other and only 96·4 % similarity to strain LMG 21919T.
Genomic relatedness between the novel Antarctic strains (representing the four different rep-PCR profile types) and their most closely related phylogenetic neighbours (F. gillisiae for rep-PCR profile types I, III and IV and F. pectinovorum and F. saccharophilum for rep-PCR profile type II) was determined by DNA–DNA hybridization. DNA was prepared according to the method of Pitcher et al. (1989) and DNA–DNA hybridizations were carried out with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989), using an HTS7000 BioAssay reader (PerkinElmer) for fluorescence measurements. The hybridization temperature was 32 °C and reciprocal experiments were performed for every pair of strains. The hybridization level between strains LMG 21915T, LMG 21916, LMG 21917 and LMG 21474 of rep-PCR profile type I was 93·6–97·7 %, indicating that the 14 strains of rep-PCR profile type I belong to a single species (Wayne et al., 1987). Hybridization values of LMG 21915T with its nearest phylogenetic neighbours, F. gillisiae (LMG 21422T), F. xanthum (LMG 8372T) and LMG 21922T, were respectively 28·9, 18·4 and 28·4 %, indicating that the strains of rep-PCR profile type I represent a novel Flavobacterium species, for which the name Flavobacterium degerlachei sp. nov. is proposed.
High hybridization values (81·1–84·7 %) were obtained between strains LMG 21919T, LMG 21920 and LMG 21921 of rep-PCR profile type II. The low hybridization level (13·2–16·1 %) between LMG 21919T and its nearest phylogenetic neighbours, F. pectinovorum (LMG 4031T) and F. saccharophilum (LMG 8384T), reveals that the three strains of rep-PCR profile type II constitute a novel species, for which the name Flavobacterium micromati sp. nov. is proposed.
Hybridization results between strains LMG 21922T, LMG 21923, LMG 21924 and LMG 21925 of rep-PCR profile types III and IV (82·5–91·2 %) showed that the strains of these two different rep-PCR profile types represent a single species that is clearly different from related Flavobacterium species. LMG 21922T showed only 52 % hybridization with F. gillisiae (LMG 21422T) and 4·1 % with F. xanthum (LMG 8372T); the name Flavobacterium frigoris sp. nov. is proposed for this species.
Differences between reciprocal experiments were <14 %. These results show clearly that the novel Antarctic isolates are genotypically distinct from related Flavobacterium species, although the isolates share >97 % (up to 98·7 %) 16S rRNA gene sequence similarity with their closest phylogenetic neighbours, and that they constitute three novel species within the genus Flavobacterium.
DNA G+C contents of the Antarctic strains were determined by using an HPLC-based method as described by Van Trappen et al. (2003). The DNA G+C contents of strains LMG 21915T, LMG 21916, LMG 21917, LMG 21474 and LMG 21918 of F. degerlachei sp. nov. are 34·2, 34·2, 34·1, 33·8 and 34·2 mol%, respectively. The DNA G+C contents of strains LMG 21919T, LMG 21920 and LMG 21921 of F. micromati sp. nov. are 34·4, 33·1 and 33·1 mol%, respectively, and those of strains LMG 21922T, LMG 21923, LMG 21924 and LMG 21925 of F. frigoris sp. nov. are 34·5, 34·2, 34·4 and 33·8 mol%, respectively. These values are consistent with the DNA G+C contents of members of the genus Flavobacterium, which range from 30 to 37 mol% (Bernardet et al., 1996; Van Trappen et al., 2003).
Cellular fatty acid patterns of the Antarctic strains are based on data generated by Van Trappen et al. (2002). The strains showed similar fatty acid profiles (Table 2); major constituents included C15 : 0, iso-C15 : 0, iso-C16 : 0 3-OH and summed feature 3 (which comprises iso-C15 : 0 2-OH, C16 : 17c or both). Strains of F. degerlachei and F. frigoris also possessed relatively large amounts of anteiso-C15 : 0 and C15 : 16c, whilst strains of F. micromati showed relatively large amounts of iso-C16 : 0. Hydroxylated fatty acids and iso- and anteiso-branched fatty acids were also present as minor components. Their fatty acid profiles resemble those determined for other Flavobacterium species (Bernardet et al., 1996), but differ in the relative amounts of anteiso-C15 : 0, iso-C15 : 0 and iso-C17 : 0 3-OH.
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) after 14 days were tested. Cells were tested for their Gram-stain reaction and for catalase and oxidase activities. Tests in the commercial API ZYM, API 20NE and API 20E systems (bioMérieux) were generally performed according to the instructions of the manufacturer. API ZYM tests were read after 4 h incubation at 20 °C and other API tests were read after 48 h at 20 °C. Congo red absorption (Bernardet et al., 2002), production of flexirubin-type pigments (Reichenbach, 1989), presence of gliding motility, degradation of casein and chitin (Reichenbach & Dworkin, 1981), alginate (West & Colwell, 1984), DNA [using DNA agar (Difco), supplemented with 0·01 % toluidine blue (Merck)], pectin (Paton, 1959), starch and L-tyrosine (Barrow & Feltham, 1993), production of brown diffusible pigment on L-tyrosine agar and precipitation of egg-yolk agar (Barrow & Feltham, 1993) were also investigated; reactions were read after 5 days. Hydrolysis of CM-cellulose was tested in Anacker & Ordal's broth (Anacker & Ordal, 1955), gelidified with 3 % high-viscosity CM-cellulose sodium salt (Sigma). This medium was stab-inoculated and liquefaction of the medium within 7 days was scored as a positive reaction. Growth at different temperatures was assessed after 5 days incubation. Salt tolerance was tested on R2A medium supplemented with 1–10 % NaCl after 14 days incubation.
The strains showed typical morphological characteristics of the genus Flavobacterium (Bernardet et al., 2002) and their physiological and biochemical characteristics are given in the species descriptions. F. degerlachei sp. nov., F. micromati sp. nov. and F. frigoris sp. nov. can be differentiated clearly from each other and from related Flavobacterium species by several phenotypic characteristics (Table 3).
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Description of Flavobacterium degerlachei sp. nov.
Flavobacterium degerlachei (de.ger.lach'e.i. N.L. gen. n. degerlachei of Adrien de Gerlache, in honour of the Belgian pioneer who conducted the first scientific expedition to Antarctica in 1897–1899).
Cells are Gram-negative, short rods (<1x3–4 µm) that often form pairs or short chains. Gliding motility is not observed. Growth occurs at 5–30 °C with an optimal growth temperature of 20 °C, whereas no growth occurs at 37 °C. Yellow, convex, translucent colonies with entire margins and a diameter of 1–3 mm are formed on R2A plates after 6 days incubation. Colonies on Anacker & Ordal's agar are flat, round with entire margins and 0·5–1·0 mm in diameter after 14 days incubation. Growth also occurs on trypticase soy agar, nutrient agar and marine agar; colonies do not adhere to the agar. Aesculin and starch are degraded. Catalase and oxidase tests are positive. Growth is observed (API 20NE) on glucose, mannose and maltose, whereas no growth is detected on arabinose, mannitol, N-acetylglucosamine, gluconate, caprate, adipate, malate, citrate or phenylacetate. Acids are not produced from carbohydrates (API 20E). Agar, alginate, pectin, chitin, casein, CM-cellulose, DNA, gelatin, tyrosine and urea are not degraded. Congo red is not absorbed and no flexirubin-type pigments are present. No production of brown diffusible pigment occurs on L-tyrosine agar and no precipitate is formed on egg-yolk agar. Tests for indole production, citrate utilization, nitrate reduction, Voges–Proskauer reaction and hydrogen sulfide production are negative. None of the strains shows activity for the enzymes arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase (API 20E), lipase (C14), -chymotrypsin, trypsin, -galactosidase, -galactosidase, -glucuronidase, -mannosidase or -fucosidase (API ZYM). Weak enzymic activity is observed for cystine arylamidase, medium activity is observed for esterase (C4), esterase lipase (C8), -glucosidase, -glucosidase and N-acetyl -glucosaminidase, and strong activity is observed for alkaline phosphatase, leucine arylamidase, valine arylamidase, acid phosphatase and naphthol-AS-BI-phosphohydrolase (API ZYM). Cells contain the fatty acids C15 : 0, anteiso-C15 : 0, iso-C15 : 0, C15 : 16c, iso-C16 : 0 3-OH, C17 : 16c and summed feature 3 (which comprises iso-C15 : 0 2-OH, C16 : 17c or both) as the main constituents. Growth occurs in 0–5 % NaCl but not in 10 % NaCl, indicating that the strains are not halophilic, but are moderately halotolerant. DNA G+C content is 33·8–34·2 mol%.
The type strain is LMG 21915T (=DSM 15718T). Isolated from microbial mats from Lakes Ace and Pendant in the Vestfold Hills and Lake Reid in the Larsemann Hills, Antarctica.
Description of Flavobacterium micromati sp. nov.
Flavobacterium micromati (mi.cro.mat'i. N.L. gen. n. micromati referring to the MICROMAT project).
Cells are Gram-negative, short rods (<1x3–4 µm); gliding motility is not observed. Growth occurs at 5–20 °C, very weak growth is observed at 25 °C and no growth occurs at 30 °C. Orange–red, convex, translucent colonies with entire margins and a diameter of 1–3 mm are formed on R2A plates after 6 days incubation. Colonies on Anacker & Ordal's agar are flat, round with entire margins and 0·5–1·0 mm in diameter after 14 days incubation. Growth also occurs on trypticase soy agar (weak), nutrient agar and marine agar (weak). Colonies do not adhere to the agar. Aesculin is degraded. Catalase and oxidase tests are positive. Growth on carbohydrates (API 20NE) is not observed and acids are not produced from carbohydrates (API 20E). Voges–Proskauer reaction is positive for all strains. Agar, alginate, pectin, chitin, casein, CM-cellulose, DNA, gelatin, tyrosine, starch and urea are not degraded. Congo red is not absorbed and no flexirubin-type pigments are present. No production of brown diffusible pigment occurs on L-tyrosine agar and no precipitate is formed on egg-yolk agar. Tests for indole production, citrate utilization, nitrate reduction and hydrogen sulfide production are negative. None of the strains shows activity for the enzymes arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase (API 20E), lipase (C14), cystine arylamidase, -chymotrypsin, trypsin, -galactosidase, -galactosidase, -glucuronidase, -glucosidase, N-acetyl -glucosaminidase, -mannosidase or -fucosidase (API ZYM). Medium enzymic activity is observed for esterase (C4) and esterase lipase (C8) and strong activity is observed for alkaline phosphatase, leucine arylamidase, valine arylamidase, acid phosphatase, naphthol-AS-BI-phosphohydrolase and -glucosidase (API ZYM). Cells contain the fatty acids C15 : 0, anteiso-C15 : 0, iso-C15 : 0, C15 : 16c, iso-C16 : 0, iso-C16 : 0 3-OH and summed feature 3 (which comprises iso-C15 : 0 2-OH, C16 : 17c or both) as the main constituents. Growth occurs in 0–2 % NaCl, but not in 5 % NaCl. DNA G+C content is 33·1–34·4 mol%.
The type strain is LMG 21919T (=CIP 108161T). Isolated from microbial mats from Lake Grace in the Vestfold Hills and Lake Fryxell in the McMurdo Dry Valleys, Antarctica.
Description of Flavobacterium frigoris sp. nov.
Flavobacterium frigoris (fri'go.ris. L. gen. n. frigoris of the cold).
Cells are Gram-negative, short rods (<1x4–6 µm); gliding motility is not observed. Growth occurs at 5–20 °C, weak growth is observed at 25 °C and no growth occurs at 37 °C. Yellow, convex, translucent colonies with entire margins and a diameter of 2–5 mm are formed on R2A plates after 6 days incubation. Colonies on Anacker & Ordal's agar are flat, round with entire margins and 0·5–1·0 mm in diameter after 14 days incubation. Growth also occurs on trypticase soy agar and marine agar, but not on nutrient agar. Colonies do not adhere to the agar. Aesculin, casein, tyrosine and starch are degraded. Catalase and oxidase tests are positive. Growth on carbohydrates (API 20NE) is observed for glucose, mannose and maltose; acids are not produced from carbohydrates (API 20E). Agar, alginate, pectin, chitin, CM-cellulose, DNA, gelatin and urea are not degraded. Congo red is not absorbed and no flexirubin-type pigments are present. No production of brown diffusible pigment occurs on L-tyrosine agar and no precipitate is formed on egg-yolk agar. Tests for indole production, citrate utilization, Voges–Proskauer reaction and hydrogen sulfide production are negative. Strain LMG 21924 is able to reduce nitrate to nitrite. None of the strains shows activity for the enzymes arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase (API 20E), -chymotrypsin, trypsin, -galactosidase, -galactosidase, -glucuronidase, -mannosidase or -fucosidase (API ZYM). Weak enzymic activity is observed for cystine arylamidase, medium activity is observed for esterase (C4), esterase lipase (C8) and N-acetyl -glucosaminidase, and strong activity is observed for alkaline phosphatase, leucine arylamidase, valine arylamidase, acid phosphatase, naphthol-AS-BI-phosphohydrolase and -glucosidase (API ZYM). Only strain LMG 21924 showed medium activity for -glucosidase and strain LMG 21922 for lipase (C14). Cells contain the fatty acids C15 : 0, anteiso-C15 : 0, iso-C15 : 0, C15 : 16c, iso-C16 : 0, iso-C16 : 0 3-OH and summed feature 3 (which comprises iso-C15 : 0 2-OH, C16 : 17c or both) as the main constituents. Growth occurs in 0–5 % NaCl but not in 10 % NaCl, indicating that the strains are not halophilic, but are moderately halotolerant. DNA G+C content of the strains is 33·8–34·5 mol%.
The type strain is LMG 21922T (=DSM 15719T). Isolated from microbial mats from Lakes Watts, Grace and Druzhby in the Vestfold Hills, Lake Fryxell in the McMurdo Dry Valleys and Lake Reid in the Larsemann Hills, Antarctica.
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ACKNOWLEDGEMENTS |
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