HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) rep-PCR profiles Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Van Trappen, S. Articles by Swings, J. Search for Related Content PubMed PubMed Citation Articles by Van Trappen, S. Articles by Swings, J. Agricola Articles by Van Trappen, S. Articles by Swings, J.

Glaciecola polaris sp. nov., a novel budding and prosthecate bacterium from the Arctic Ocean, and emended description of the genus Glaciecola

¹ Laboratorium voor Microbiologie, Vakgroep Biochemie, Fysiologie en Microbiologie, Universiteit Gent, Gent, Belgium
² Alfred-Wegener-Institut für Polar- und Meeresforschung, Bremerhaven, Germany
³ Zhejiang Wanli University, Ningbo, China
⁴ BCCM/LMG Culture Collection, Universiteit Gent, Gent, Belgium

Correspondence
Stefanie Van Trappen
stefanie.vantrappen{at}UGent.be

	ABSTRACT

TOP ABSTRACT MAIN TEXT REFERENCES

 
Four strains of cold-adapted, strictly aerobic and facultative oligotrophic bacteria were isolated from polar seas and investigated using a polyphasic taxonomic approach. Two strains (LMG 21857^T and LMG 21854) derive from Arctic sea water whereas the other two strains (LMG 21855 and LMG 21858) were isolated from Antarctic sea water. Phylogenetic analysis based on 16S rRNA gene sequences indicated that these strains belong to the -subclass of the Proteobacteria and are related to the genus Glaciecola, with 98·0–99·7 % sequence similarity to Glaciecola mesophila and 94·2–95·3 % sequence similarity to Glaciecola punicea, their nearest phylogenetic neighbours. Two strains (LMG 21855 and LMG 21858) were identified as G. mesophila, whereas DNA–DNA hybridization results and differences in phenotypic characteristics showed that the other two strains (LMG 21857^T and LMG 21854) constitute a novel species within the genus Glaciecola, with a DNA G+C content of 44·0 mol%. The isolates are Gram-negative, chemoheterotrophic, motile, rod-shaped cells that are psychrotolerant and moderately halophilic. Buds can be produced on mother cells and on prosthecae. Branch formation of prosthecae occurs. Whole-cell fatty acid profiles of the isolates are very similar and include C_{16 : 0} and C_{16 : 1}7c as the major fatty acid components. On the basis of genotypic and phenotypic properties, a novel species of the genus Glaciecola is described, for which the name Glaciecola polaris sp. nov. is proposed, with isolate LMG 21857^T (=CIP 108324^T=ARK 150^T) as the type strain. An emended description of the genus Glaciecola is presented.

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains LMG 21857^T and LMG 21855 are AJ293820 and AJ548479, respectively.

Normalized rep-PCR profiles (GTG₅ primer) and a dendrogram derived from the UPGMA clustering of the profiles are available as supplementary material in IJSEM Online.

	MAIN TEXT

TOP ABSTRACT MAIN TEXT REFERENCES

 
The genus Glaciecola was proposed by Bowman et al. (1998) for two groups of psychrophilic bacteria isolated from sea-ice diatom assemblages from the coastal areas of eastern Antarctica and forms a separate lineage within the -subclass of the Proteobacteria, being distantly related to Alteromonas macleodii. Recently, another species of the genus Glaciecola was described, Glaciecola mesophila, isolated from marine invertebrate specimens (Romanenko et al., 2003). Many genera of this class of Proteobacteria (Alteromonas, Pseudoalteromonas, Glaciecola, Idiomarina and Colwellia) are common inhabitants of the marine part of the biosphere and have very diverse habitats, e.g. coastal and open-water areas, deep-sea and hydrothermal vents, marine sediments and sea ice (Mikhailov et al., 2002).

In another study, we reported that seven Antarctic strains belong to a novel species within the genus Alteromonas, Alteromonas stellipolaris (Van Trappen et al., 2004b). Together with the novel Glaciecola species described here, they all belong to the group of novel budding and prosthecate bacteria from the -subclass of the Proteobacteria. It is now evident that budding and prosthecate bacteria are abundant in marine and polar environments (Weiner et al., 2000; Labrenz et al., 1998, 1999). Moreover, bud and prostheca formation is a common strategy for rod-shaped bacteria to enhance their surface-to-volume ratio, thus enabling efficient substrate uptake in oligotrophic habitats (van Gemerden & Kuenen, 1984).

During expeditions in the Arctic (Tan & Rüger, 1991) and Antarctic seas (Tan & Rüger, 1999), facultative oligotrophic and psychrophilic/psychrotolerant bacteria were isolated. These strains (173) have been previously analysed by means of the Biolog system (substrate utilization patterns) (Tan, 1997; Tan & Rüger, 1999), fatty acid analysis and 16S rRNA gene sequence analysis of representatives (Mergaert et al., 2001). They belong to six metabolic groups and eight different fatty acid clusters containing 2–59 strains. In the meantime, additional strains (56) were isolated using the same methods and were also analysed using the Biolog system and fatty acid analysis. The novel strains belong to fatty acid clusters B, C, D, E and F (as delineated in Mergaert et al., 2001), and three new fatty acid clusters (I, J and K; S. Van Trappen, unpublished results) were found. The genomic diversity of the 19 strains from fatty acid clusters E and F and two related unclustered strains was further investigated (see also Van Trappen et al., 2004b) and these strains were arranged in similarity groups based upon the results of repetitive sequence-based (rep)-PCR fingerprinting using the GTG₅ primer (Versalovic et al., 1991; Rademaker & de Bruijn, 1997; Rademaker et al., 2000). Numerical analysis was carried out using the BIONUMERICS software package (Applied Maths; available at http://www.applied-maths.com), as described by the same authors. One Arctic cluster (LMG 21857^T, LMG 21854) and one Antarctic cluster (LMG 21855, LMG 21858), each containing two strains and belonging to FAA cluster F and having almost identical rep-PCR profiles, could be delineated (see supplementary figure in IJSEM Online); 16S rRNA gene sequence analysis revealed that they belong to the genus Glaciecola within the -subclass of the Proteobacteria.

Strains were isolated from sea water after enrichment in dialysis chambers as previously described (Tan, 1986, 1997). The strains investigated were LMG 21857^T (=CIP 108324^T=ARK 150^T) and LMG 21854 (=ARK 149), isolated from Arctic sea water, and LMG 21855 (=ANT 12a) and LMG 21858 (=ANT 12b), from Antarctic sea water. The reference strains Glaciecola punicea LMG 21426^T, Glaciecola pallidula LMG 21427^T and G. mesophila LMG 22017^T were included in some experiments. Strains were routinely cultivated on marine agar 2216 (Difco) at 20 °C for 48 h, or, for strains LMG 21426^T and LMG 21427^T, on marine agar 2216 at 10 °C for 6 days, or, for strain LMG 22017^T, on marine agar 2216 at 28 °C for 24 h, unless mentioned otherwise.

Small-scale DNA extracts were prepared using the method of Pitcher et al. (1989) and the almost-complete 16S rRNA gene sequences (1485 nt) of strains LMG 21857^T, LMG 21854, LMG 21855 and LMG 21858 were amplified by a PCR using conserved primers (Coenye et al., 1999). PCR products were purified using a QIAquick PCR Purification kit (Qiagen) according to the instructions of the manufacturer. Sequence analysis was performed as described earlier (Van Trappen et al., 2004a). Evolutionary distances were calculated using the algorithm of Jukes–Cantor (Jukes & Cantor, 1969) and a phylogenetic tree (shown in Fig. 1) was constructed using the neighbour-joining method (Saitou & Nei, 1987) with the TREECON program (Van de Peer & De Wachter, 1994). Dendrograms obtained using maximum-parsimony and maximum-likelihood analyses showed essentially the same topography (data not shown).

View larger version (43K): [in this window] [in a new window]   Fig. 1. Neighbour-joining dendrogram showing the estimated phylogenetic relationships of the Arctic and Antarctic isolates and other marine chemoheterotrophs of the -subclass of the Proteobacteria. Bootstrap values (percentages of 500 replicates) greater than 50 % are shown. The GenBank/EMBL/DDBJ accession number for each reference strain is shown in parentheses. Bar, 1 nucleotide substitution per 10 nucleotides.

The genomic relatedness between strains LMG 21857^T, LMG 21855 and the most closely related strains, G. mesophila LMG 22017^T and G. punicea LMG 21426^T, was determined by DNA–DNA hybridizations. DNA was prepared according to the method of Pitcher et al. (1989); DNA–DNA hybridizations were carried out with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989), using an HTS7000 Bio Assay Reader (Perkin Elmer) for the fluorescence measurements. The hybridization temperature was 35 °C and reciprocal experiments were performed for every pair of strains. The hybridization level between strain LMG 21857^T and G. mesophila LMG 22017^T and G. punicea LMG 21426^T was 17·2 and 4·0 %, respectively, whereas the DNA–DNA binding value between LMG 21857^T and LMG 21855 was 23·4 %. The hybridization level between strain LMG 21855 and G. mesophila LMG 22017^T and G. punicea LMG 21426^T was 67·7 and 6·0 %, respectively. Differences between reciprocal experiments were less than 10 %. DNA–DNA hybridizations between strains of the same rep-PCR cluster were not performed since Versalovic et al. (1994) have shown that strains with the same rep-PCR profile are always closely related (as confirmed by several authors, e.g. Rademaker & De Bruijn, 1997). These results suggest that the two Arctic isolates are genotypically distinct from G. mesophila and G. punicea (their closest neighbours in phylogenetic terms) and constitute a novel species within the genus Glaciecola. The two Antarctic isolates are closely related to G. mesophila, showing a DNA–DNA reassociation value near 70 %, which is generally accepted as the threshold for species delineation (Wayne et al., 1987).

DNA G+C contents of the Arctic and Antarctic strains were determined using an HPLC method, as described by Van Trappen et al. (2003). The DNA G+C contents of strains LMG 21857^T, LMG 21854, LMG 21855 and LMG 21858 are 44·2, 43·6, 43·9 and 44·2 mol%, respectively. These values are consistent with the G+C content of the genus Glaciecola, which ranges between 40 and 46 mol% (Bowman et al., 1998).

The cellular fatty acid patterns of the polar strains are based on the data generated by Mergaert et al. (2001) or were determined as described by the same authors. The Arctic strains show very similar fatty acid profiles and the mean composition is as follows: 3·1 % C_{12 : 0}, 5·5 % C_{12 : 0} 3-OH, 4·1 % C_{14 : 0}, 2·0 % C_{15 : 0}, 23·3 % C_{16 : 0}, 1·7 % C_{16 : 0} 2-OH, 2·0 % C_{16 : 1} 2-OH, 2·6 % C_{17 : 1}8c, 4·8 % C_{18 : 1}7c, 1·4 % C_{18 : 0} 10-methyl and 41·7 % summed feature 3, which comprises iso-C_{15 : 0} 2-OH and/or C_{16 : 1}7c. The Antarctic strains have fatty acid patterns very similar to those of strains KMM 241^T and KMM 642 (G. mesophila), with C_{16 : 0}, C_{16 : 1}7c, C_{17 : 1}8c and C_{18 : 1}7c as the dominant fatty acids. Hydroxylated fatty acids and iso-branched fatty acids were also present as minor components or at trace levels in the Arctic strains. The fatty acid profiles of the polar strains clearly resemble those determined for other marine genera of the -subclass of the Proteobacteria, e.g. Alteromonas, Pseudoalteromonas and Glaciecola (Ivanova et al., 2000).

The growth of the strains at different temperatures (5–37 °C) was tested on marine agar 2216, whereas salt tolerance was tested on R2A agar (Difco), supplemented with 1–20 % (w/v) NaCl, at 20 °C. Biochemical characteristics were determined using standard protocols (Smibert & Krieg, 1994; West & Colwell, 1984; Reichenbach & Dworkin, 1981; Bowman et al., 1998; Van Trappen et al., 2003) and API kits (API 20E, API 20NE, API ZYM and API 32ID; bioMérieux). Bacterial suspensions were made in sterile, chilled sea water, and marine agar was used as the basal medium. For Biolog GN2 microplates, the bacteria were grown on peptone/yeast extract/glucose (PYG) agar at 20 °C for 5 days; the cells were harvested and suspended in ‘inoculating fluid’. The salinity of the ‘inoculating fluid’ was adjusted to 26 parts per thousand with NaCl. The microplates were incubated at 20 °C and substrate utilizations were measured after 3–28 days at 590 nm with an eight-channel photometer (Spectra 2; SLT Labinstruments).

The Antarctic strains are Gram-negative, rod-shaped cells (0·4 µm in width and 2–3 µm in length) and are flagellated. Buds and prosthecae can be produced (Fig. 2). The strains are able to grow between 5 and 30 °C, whereas no growth occurs at 37 °C; growth is supported on R2A agar with up to 10 % (w/v) NaCl. The colonies have a mucoid consistency, show reactions very similar to those of strains KMM 241^T and KMM 642 of G. mesophila and reduce nitrate. They differ from these strains in the degradation of agar and the utilization of D-fructose, D-trehalose, L-glutamate and L-proline, and the Antarctic strains grow at 4 °C and in 10 % (w/v) NaCl (see Table 1). Antarctic strains LMG 21855 and LMG 21858 are identified as G. mesophila since there are only a few phenotypic differences, which could be due to the different protocols used, and DNA–DNA hybridization results together with the 16S rRNA gene sequence similarities also support the notion that these Antarctic isolates are very closely related to G. mesophila.

View larger version (106K): [in this window] [in a new window]   Fig. 2. Electron micrographs of negatively stained preparations of cells of strains LMG 21855 (a–c) and LMG 21858 (d), showing flagella (F), prosthecae (P), buds (B) and extracellular products (EPs). Colonies used for analysis were grown on PYG agar at 12 °C for 7 days. Cells were stained with 1 % (w/v) uranyl acetate in 0·4 % (w/v) sucrose. Bars, 300 nm.

View larger version (69K): [in this window] [in a new window]   Fig. 3. Electron micrographs of negatively stained preparations of cells of strain LMG 21857T, showing flagella (F), prosthecae (P) and buds (B). For methods, see the legend to Fig. 2.

Emended description of the genus Glaciecola Bowman et al. 1998 emend. Van Trappen et al.
The description is as described by Bowman et al. (1998), with the following additional morphological features. When grown on marine or PYG agar at low temperatures (12–20 °C) for 3 days or more, some strains can produce buds and prosthecae (see Figs 2, 3 and 4).

View larger version (57K): [in this window] [in a new window]   Fig. 4. Electron micrographs of negatively stained preparations of cells of G. punicea LMG 21426T (a), G. pallidula LMG 21427T (b) and G. mesophila LMG 22017T (c), showing prosthecae (P), buds (B) and extracellular products (EPs). Colonies used for analysis were grown on PYG agar at 20 °C for 3 days (G. mesophila) or on marine agar at 12 °C for 21 days (G. punicea) or 12 days (G. pallidula), respectively. Cells were stained with 1 % (w/v) uranyl acetate in 0·4 % (w/v) sucrose. Bars, 1000 nm.

Cells are Gram-negative, short rods (0·4x2–3 µm) that are motile by means of a polar or subpolar flagellum. Buds can be produced on mother cells or on prosthecae. Prostheca formation is peritrichous and prosthecae can be branched (Figs 2, 3 and 4). They form non-pigmented, circular, low convex, shiny and opaque colonies that are not adherent to agar and which have entire margins and a diameter of 1–4 mm on marine agar 2216 plates after 7 days incubation at 20 °C. Growth occurs on marine and PYG agar and there is a slight growth on nutrient agar, but there is no growth on trypticase soy agar or R2A agar. The temperature range for growth is 5–30 °C, whereas no growth occurs at temperatures of 37 °C or above; growth is observed on R2A agar with up to 10 % (w/v) NaCl, indicating that the cells are moderately halophilic and psychrotolerant. There is no evidence for growth under anaerobic conditions, and the catalase and cytochrome oxidase tests are positive. Tests positive for the degradation of starch, aesculin and DNA, and precipitation on egg-yolk agar occurs. -Galactosidase activity is detected for both strains. They are able to utilize -cyclodextrin, dextrin, glycogen, Tween 40, Tween 80, D-arabitol, cellobiose, D-fructose, D-galactose, gentiobiose, -D-glucose, -D-lactose, lactulose, maltose, D-mannitol, D-mannose, D-melibiose, methyl -D-glucoside, D-raffinose, sucrose, D-trehalose, D-sucrose, furanose, methylpyruvate, acetic acid, -hydroxybutyric acid, propionic acid, L-alanine, L-alanyl-glycine, L-glutamic acid, glycyl-L-glutamic acid, L-leucine, L-pyroglutamic acid and salicin. Both strains are negative in tests for indole and acetoin production, in the Voges–Proskauer test and in tests for citrate utilization, hydrolysis of urate, nitrate reduction and the production of hydrogen sulfide. No growth is observed on arabinose, N-acetylglucosamine, caprate, adipate, malate, citrate, phenylacetate, L-fucose, D-sorbitol, valerate, histidine, 2-ketogluconate, 3-hydroxybutyrate, 4-hydroxybenzoate, rhamnose, D-ribose, inositol, itaconate, suberate, malonate, DL-lactate, 5-ketogluconate, 3-hydroxybenzoate, L-serine, alaninamide, L-threonine or glycerol. No acids are produced from the carbohydrates glucose, mannitol, inositol, sorbitol, rhamnose, sucrose, melibiose, amygdalin or arabinose and tests for the degradation of alginate, chitin, casein, gelatin and urea are negative. There is no arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase or tryptophan deaminase activity. There is no activity for the enzymes lipase (C14), cystine arylamidase, -chymotrypsin, -glucuronidase, N-acetyl--glucosaminidase, -mannosidase or -fucosidase. For both strains, low activity (score 1) is obtained for valine arylamidase, trypsin, -glucosidase and -glucosidase, medium activity (score 2 or 3) is observed for esterase (C4), esterase lipase (C8), acid phosphatase, naphthol-AS-BI-phosphohydrolase and -galactosidase, and high activity (score 4 or 5) is observed for alkaline phosphatase and leucine arylamidase. Cells contain fatty acids C_{16 : 0} and summed feature 3 (iso-C_{15 : 0} 2-OH and/or C_{16 : 1}7c) as the main constituents. The DNA G+C content is 44·0 mol%.

The type strain is LMG 21857^T (=ARK 150^T=CIP 108324^T). Isolated from the Arctic Ocean.

	ACKNOWLEDGEMENTS

 
This work was funded by the ‘Bijzonder Onderzoeksfonds' (BOF), Universiteit Gent, Belgium. T.-L. T. and J. Y. are grateful to A. Mädler and S. Spahic for technical assistance.

	REFERENCES

TOP ABSTRACT MAIN TEXT REFERENCES

 
Bowman, J. P., McCammon, S. A., Brown, J. L. & McMeekin, T. A. (1998). Glaciecola punicea gen. nov., sp. nov. and Glaciecola pallidula gen. nov., sp. nov. psychrophilic bacteria from Antarctic sea-ice habitats. Int J Syst Bacteriol 48, 1213–1222.[Abstract/Free Full Text]

Coenye, T., Falsen, E., Vancanneyt, M., Hoste, B., Govan, J. R., Kersters, K. & Vandamme, P. (1999). Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol 49, 405–413.[Abstract/Free Full Text]

Ezaki, T., Hashimoto, Y. & Yabuuchi, E. (1989). Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39, 224–229.[Abstract/Free Full Text]

Ivanova, E. P., Zhukova, N. V., Svetashev, V. I., Gorshkova, N. M., Kurilenko, V. V., Frolova, G. M. & Mikhailov, V. V. (2000). Evaluation of phospholipid and fatty acid compositions as chemotaxonomic markers of Alteromonas-like proteobacteria. Curr Microbiol 41, 341–345.[CrossRef][Medline]

Jukes, T. H. & Cantor, C. R. (1969). Evolution of protein molecules. In Mammalian Protein Metabolism, pp. 21–132. Edited by H. N. Munro. New York: Academic Press.

Labrenz, M., Collins, M. D., Lawson, P. A., Tindall, B. J., Braker, G. & Hirsch, P. (1998). Antarctobacter heliothermus gen. nov., sp. nov., a budding bacterium from hypersaline and heliothermal Ekho Lake. Int J Syst Bacteriol 48, 1363–1372.[Abstract/Free Full Text]

Labrenz, M., Collins, M. D., Lawson, P. A., Tindall, B. J., Schumann, P. & Hirsch, P. (1999). Roseovarius tolerans gen. nov., sp. nov., a budding bacterium with variable bacteriochlorophyll a production from hypersaline Ekho Lake. Int J Syst Bacteriol 49, 137–147.[Abstract/Free Full Text]

Mergaert, J., Verhelst, A., Cnockaert, M. C., Tan, T.-L. & Swings, J. (2001). Characterization of facultative oligotrophic bacteria from polar seas by analysis of their fatty acids and 16S rDNA sequences. Syst Appl Microbiol 24, 98–107.[CrossRef][Medline]

Mikhailov, V. V., Romanenko, L. A. & Ivanova, E. P. (2002). The genus Alteromonas and related Proteobacteria. In The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community. Edited by M. Dworkin, E. Rosenberg, K. H. Schleifer & E. Stackebrandt. New York: Springer.

Pitcher, D. G., Saunders, N. A. & Owen, R. J. (1989). Rapid extraction of bacterial genomic DNA with guanidinium thiocyanate. Lett Appl Microbiol 8, 151–156.

Rademaker, J. L. W. & de Bruijn, F. J. (1997). Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer assisted pattern analysis. In DNA Markers: Protocols, Applications and Overviews, pp. 151–171. Edited by G. Caetano-Anollés & P. M. Gresshoff. New York: Wiley.

Rademaker, J. L. W., Hoste, B., Louws, F. J., Kersters, K., Swings, J., Vauterin, L., Vauterin, P. & de Bruijn, F. J. (2000). Comparison of AFLP and rep-PCR genomic fingerprinting with DNA–DNA homology studies: Xanthomonas as a model system. Int J Syst Evol Microbiol 50, 665–677.[Abstract]

Reichenbach, H. & Dworkin, M. (1981). Introduction to the gliding bacteria. In The Prokaryotes, vol. 1, pp. 315–327. Edited by M. P. Starr, H. Stolp, H. G. Trüper, A. Balows & H. G. Schlegel. Berlin: Springer.

Romanenko, L. A., Zhukova, N. V., Rohde, M., Lysenko, A. M., Mikhailov, V. V. & Stackebrandt, E. (2003). Glaciecola mesophila sp. nov., a novel marine agar-digesting bacterium. Int J Syst Evol Microbiol 53, 647–651.[Abstract/Free Full Text]

Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.[Abstract]

Smibert, R. M. & Krieg, N. R. (1994). Phenotypic characterization. In Methods for General and Molecular Microbiology, pp. 611–654. Edited by P. Gerhardt, R. G. E. Murray, W. A. Wood & N. R. Krieg. Washington, DC: American Society for Microbiology.

Tan, T. L. (1986). Construction and use of a dialysis chamber for investigating in situ the toxicity of heavy metals on bacteria. IFREMER Actes Colloq 3, 589–595.

Tan, T. L. (1997). Biolog metabolic fingerprints for clustering marine oligotrophic bacteria from polar regions. In Microbial Communities – Functional versus Structural Approaches, pp. 161–170. Edited by H. Insam & A. Rangger. Berlin: Springer.

Tan, T. L. & Rüger, H. J. (1991). Biomass and nutritional requirements of psychrotrophic bacterial communities in Fram Strait and Western Greenland Sea. Kiel Meeresforsch Sonderh 8, 219–224.[Medline]

Tan, T. L. & Rüger, H. J. (1999). Enrichment, isolation, and Biolog metabolic fingerprints of oligotrophic bacteria from the Antarctic Ocean. Arch Hydrobiol Spec Issues Adv Limnol 54, 255–272.

Van de Peer, Y. & De Wachter, R. (1994). TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10, 569–570.[Free Full Text]

van Gemerden, H. & Kuenen, J. G. (1984). Strategies for growth and evolution of microorganisms in oligotrophic habitats. In Heterotrophic Activity in the Sea (Nato Conference Series IV. Marine Sciences), vol. 15, pp. 25–54. Edited by J. E. Hobbie & P. J. Williams. New York: Plenum.

Van Trappen, S., Mergaert, J. & Swings, J. (2003). Flavobacterium gelidilacus sp. nov., isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 53, 1241–1245.[Abstract/Free Full Text]

Van Trappen, S., Vandecandelaere, I., Mergaert, J. & Swings, J. (2004a). 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 54, 85–92.[Abstract/Free Full Text]

Van Trappen, S., Tan, T.-L., Yang, J., Mergaert, J. & Swings, J. (2004b). Alteromonas stellipolaris sp. nov., a novel, budding, prosthecate bacterium from Antarctic seas, and emended description of the genus Alteromonas. Int J Syst Evol Microbiol 54, 1157–1163.[Abstract/Free Full Text]

Versalovic, J., Koeuth, T. & Lupski, J. R. (1991). Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting in bacterial genomes. Nucleic Acids Res 19, 6823–6831.[Abstract/Free Full Text]

Versalovic, J., Schneider, M., de Bruijn, F. J. & Lupski, J. R. (1994). Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5, 25–40.

Wayne, L. G., Brenner, D. J., Colwell, R. R. & 9 other authors (1987). International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37, 463–464.[Free Full Text]

Weiner, R. M., Melick, M., O'Neill, K. & Quintero, E. (2000). Hyphomonas adhaerens sp. nov., Hyphomonas johnsonii sp. nov. and Hyphomonas rosenbergii sp. nov., marine budding and prosthecate bacteria. Int J Syst Evol Microbiol 50, 459–469.[Abstract]

West, P. A. & Colwell, R. R. (1984). Identification and classification of the Vibrionaceae – an overview. In Vibrios in the Environment, pp. 285–363. Edited by R. R. Colwell. New York: Wiley.

This article has been cited by other articles:

				W. D. Jean, S.-P. Huang, T. Y. Liu, J.-S. Chen, and W. Y. Shieh Aliagarivorans marinus gen. nov., sp. nov. and Aliagarivorans taiwanensis sp. nov., facultatively anaerobic marine bacteria capable of agar degradation Int J Syst Evol Microbiol, August 1, 2009; 59(8): 1880 - 1887. [Abstract] [Full Text] [PDF]

				L.-P. Chen, H.-Y. Xu, S.-Z. Fu, H.-X. Fan, Y.-H. Liu, S.-J. Liu, and Z.-P. Liu Glaciecola lipolytica sp. nov., isolated from seawater near Tianjin city, China Int J Syst Evol Microbiol, January 1, 2009; 59(1): 73 - 76. [Abstract] [Full Text] [PDF]

				J.-J. Yong, S.-J. Park, H.-J. Kim, and S.-K. Rhee Glaciecola agarilytica sp. nov., an agar-digesting marine bacterium from the East Sea, Korea Int J Syst Evol Microbiol, May 1, 2007; 57(5): 951 - 953. [Abstract] [Full Text] [PDF]

				D.-C. Zhang, Y. Yu, B. Chen, H.-X. Wang, H.-C. Liu, X.-Z. Dong, and P.-J. Zhou Glaciecola psychrophila sp. nov., a novel psychrophilic bacterium isolated from the Arctic Int J Syst Evol Microbiol, December 1, 2006; 56(12): 2867 - 2869. [Abstract] [Full Text] [PDF]

				H. Matsuyama, T. Hirabayashi, H. Kasahara, H. Minami, T. Hoshino, and I. Yumoto Glaciecola chathamensis sp. nov., a novel marine polysaccharide-producing bacterium Int J Syst Evol Microbiol, December 1, 2006; 56(12): 2883 - 2886. [Abstract] [Full Text] [PDF]

				W. D. Jean, J.-S. Chen, Y.-T. Lin, and W. Y. Shieh Bowmanella denitrificans gen. nov., sp. nov., a denitrifying bacterium isolated from seawater from An-Ping Harbour, Taiwan. Int J Syst Evol Microbiol, October 1, 2006; 56(Pt 10): 2463 - 2467. [Abstract] [Full Text] [PDF]

				K. S. Baik, Y.-D. Park, C. N. Seong, E. M. Kim, K. S. Bae, and J. Chun Glaciecola nitratireducens sp. nov., isolated from seawater. Int J Syst Evol Microbiol, September 1, 2006; 56(Pt 9): 2185 - 2188. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) rep-PCR profiles Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Van Trappen, S. Articles by Swings, J. Search for Related Content PubMed PubMed Citation Articles by Van Trappen, S. Articles by Swings, J. Agricola Articles by Van Trappen, S. Articles by Swings, J.