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1 Laboratory of Aquatic Environmental Science, Faculty of Agriculture, Kochi University, Kochi 783-8502, Japan
2 Department of Molecular and Cellular Biology, Kochi Medical School, Kochi 783-8505, Japan
Correspondence
Masao Adachi
madachi{at}cc.kochi-u.ac.jp
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ABSTRACT |
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-Proteobacteria on the basis of nearly complete 16S rRNA gene sequences. Phylogenetic analyses showed that two strains, CFPB-A9T and CFPB-A5, are closely related to each other and that their closest relative was Jannaschia helgolandensis (95·9 % sequence similarity). These strains were Gram-negative, motile, obligately aerobic rods that required sodium ions and 2–7 % sea salts for growth and did not produce bacteriochlorophyll a. Their optimal growth temperature was 25–30 °C. The strains had Q-10 as the dominant respiratory quinone. Primary cellular fatty acid in both strains was 18 : 1
7c. The DNA G+C contents of strains CFPB-A9T and CFPB-A5 were 59·1 and 59·2 mol%, respectively. Based on physiological, biological, chemotaxonomic and phylogenetic data, the strains are considered to represent a novel species, Jannaschia cystaugens sp. nov., with type strain CFPB-A9T (=LMG 22015T=NBRC 100362T).
Published online ahead of print on 13 April 2004 as DOI 10.1099/ijs.0.03029-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Jannaschia cystaugens CFPB-A9T and CFPB-A5 are AB121782 and AB121783, respectively.
Fatty acid profiles for strains CFPB-A9T and CFPB-A5 are available as supplementary material in IJSEM Online.
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. They found a clear positive correlation between the abundance of Alex-CFPB and A. tamarense and suggested that Alex-CFPB may play a significant role in the process of encystment and bloom disintegration in the field (Adachi et al., 1999). Furthermore, Adachi et al. (2003) reported that, among the strains of the 31 Alex-CFPB isolated, a total of 14 ribotypes, from ribotype A to ribotype N, were determined by restriction fragment length polymorphism (RFLP) analysis of their partial 16S rRNA gene. They clarified that most of the Alex-CFPB belonged to the -Proteobacteria, the Roseobacter–Sulfitobacter–Silicibacter group reported by Wagner-Döbler et al. (2003), and the bacterial strains of ribotype A among them were suggested to have been dominant during the periods of bloom peak and bloom decay of A. tamarense (Adachi et al., 2003). A large number of strains from the Roseobacter–Sulfitobacter–Silicibacter group have been cultivated from various marine environments over the last few years. Strains belonging to the species Roseobacter denitrificans and Roseobacter litoralis are strict aerobes that are capable of photosynthesis using bacteriochlorophyll a (Shiba, 1991). Aerobic heterotrophs from the group include members of the genera Octadecabacter (Gosink et al., 1997), Sulfitobacter (Labrenz et al., 2000; Pukall et al., 1999; Sorokin, 1995), Sagittula (González & Moran, 1997), ‘Marinosulfonomonas’ (Holmes et al., 1997), Leisingera (Schaefer et al., 2002), Antarctobacter (Labrenz et al., 1998), Roseovarius (Labrenz et al., 1999), Ruegeria (Uchino et al., 1998), Ketogulonicigenium (Urbance et al., 2001), Roseivivax (Suzuki et al., 1999), Silicibacter (Petursdottir & Kristjansson, 1997), Staleya (Labrenz et al., 2000) and Jannaschia (Wagner-Döbler et al., 2003). Physiological characteristics of the species within these genera are diverse, ranging from degradation of lignin (González & Moran, 1997), degradation of aromatic compounds (Buchan et al., 2000), degradation of dimethyl sulfoniopropionate produced by algae and coastal vascular plants (González et al., 1999; Ledyard et al., 1993) to transformations of organic and inorganic sulfur compounds (Holmes et al., 1997; Kiene et al., 1999; Pukall et al., 1999). Here, we characterize and describe an Alex-CFPB of ribotype A, strains CFPB-A9T and CFPB-A5, from Hiroshima Bay, which may be dominant among the Alex-CFPB assemblages and potentially play an important ecological role in the process of encystment of A. tamarense in this bay.
Two bacterial strains (CFPB-A9T and CFPB-A5) were isolated from coastal sea-water samples taken at station 11 (Stn 11, depth about 22 m), a shallow coastal site in Hiroshima Bay, western Seto Inland Sea. Bacterial sampling was conducted on 28 April and 21 May 1998 according to the method described previously (Adachi et al., 1999). Strain CFPB-A9T was obtained from the diluted supernatant from a ‘most probable number (MPN)-positive well’ containing the sea-water sample from Hiroshima Bay taken on 28 April, as described previously (Adachi et al., 2003). For an MPN assay, each sea-water sample was first filtered through a glass-fibre filter and then through a 0·8 µm Millipore or 0·2 µm Nuclepore filter. The 0·8 µm filtrate was considered as the fraction containing the bulk of the planktonic bacteria (BF) and the 0·2 µm filtrate as the ‘bacteria-free’ fraction (BFF). The BF filtrate was serially diluted. BFF, BF, serially diluted BF and f/2-Si medium (Adachi et al., 1996) were each inoculated into 16 wells of 48-well disposable sterilized tissue-culture microplates (Iwaki CO). In parallel, axenic cultures of Alexandrium catenella 6ax and TNY7 in the mid-exponential phase of growth were mixed together, as described by Adachi et al. (1999). One millilitre of the mixed cell suspension was inoculated into each of the 48 microwells, mixed gently and incubated under the conditions described by Adachi et al. (1999). One month after the start of the incubation, the numbers of whole cysts formed in each well were counted under an inverted microscope (IX-FLA; Olympus). Wells in which the cyst number was more than three times higher than the mean cyst number formed in the bacteria-free wells (n=18) were regarded as ‘Alex-CFPB-positive’. One hundred microlitres of these diluted MPN-positive samples were spread onto FeTY agar plates [0·01 g iron(III) citrate l–1, 0·5 g trypticase peptone l–1, 0·05 g yeast extract l–1, 15 g agar l–1, 80 % sea water] and incubated at 20 °C for 1 month in the dark using the method described by Adachi et al. (2001). Strain CFPB-A5 was isolated directly from the sea-water sample taken on 21 May using FeTY agar under the conditions described previously (Adachi et al., 2003). The cyst formation-promoting activities (CFPAs) of CFPB-A9T and CFPB-A5, calculated using the formula CFPA=cyst number in wells inoculated with bacteria (bacterial wells)/cyst number in bacteria-free wells, were 11·6 and 8·01, respectively (Adachi et al., 2003). CFPAs of these strains were determined repeatedly using the method described previously.
Growth was typically observed for strains CFPB-A9T and CFPB-A5 after 5 days on Marine Agar 2216 (Difco) plates when incubated at 25 °C. Colonies of these two strains were circular and convex with a cream-coloured margin and a raised, dark-brown centre. Older colonies of these strains became brown. Morphological characterization was carried out using light microscopy, including phase-contrast observations. Cells were irregular rods (sizes are given in Table 1). Transmission electron microscope investigation was carried out as described by Rheims et al. (1999). White inclusion bodies were sometimes present, which were clearly not gas vesicles, as judged by transmission electron microscope investigations (Fig. 1). The two strains did not form spores. A culture of the type strain Jannaschia helgolandensis Hel 10T was obtained from NCIMB Japan Co., Ltd (Shizuoka, Japan) and was used as a reference strain. All strains were stored at –80 °C in Marine Broth 2216 (Difco) supplemented with 20 % (v/v) glycerol.
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. One drop of this suspension was added to each of the test tubes or test plates. Temperature range for growth was tested in Marine Broth 2216 at 5, 10, 15, 20, 25, 30, 37 and 45 °C. Growth was poor at 5 °C and continued up to 30 °C, with an optimum temperature range of 25–30 °C. Halotolerance was tested in LBSS medium (10·0 g tryptone l–1, 5·0 g yeast extract l–1) with 0, 1, 2, 3, 5, 7, 10 and 13 % (w/v) sea salts (Sigma) added as described by Wagner-Döbler et al. (2003). In medium devoid of sea salts, no growth of either isolate was observed. Growth was observed at sea-salt concentrations of 2–7 % (w/v), with optimum growth at 3–5 %. The pH range for growth was determined in the range 6·0–10 in steps of one pH unit using Marine Broth 2216. Growth was observed at pH 7·0–9·0, with optimum growth at pH 7·0. These tests were carried out in triplicate. Capacity for anaerobic growth was tested on Marine Agar 2216 incubated in an Anaero Pack (Mitsubishi Gas Chemical Company, Inc., Tokyo, Japan). Both strains grew strictly aerobically. The following tests were carried out according to the methods described by Gerhardt et al. (1994): Gram-staining, motility, cytochrome oxidase reaction, catalase reaction, starch hydrolysis, gelatin hydrolysis and nitrite production. Glucose fermentation was tested using the fermentation medium reported by Leifson (1963). The results are summarized in Table 1
. Physiological reactions were tested using the substrate panels of the API 20NE and API 50CH systems (bioMérieux) according to the manufacturer's specifications, except that sea salts (Sigma) were added to the inocula. For the inocula of the API 20NE and API 50CH assimilation tests, 2·8 ml of 10 % (w/v) sea salts and 7·2 ml of AUX medium were added to the 10 ml of the cell suspension corresponding to McFarland standard 1 described above. Each strip was tightly sealed with Parafilm and incubated at 25 °C for 20 days. In the physical and biochemical tests, J. helgolandensis Hel 10T was used as a reference strain. Biochemical and physiological characteristics useful for identifying and differentiating the novel isolates and J. helgolandensis are shown in Table 1.
The absorption spectra of whole cells (Shiba, 1991) and methanol extracts (Ledyard et al., 1993) of ultrasonicated cells were determined with a Hitachi F-2000 spectrophotometer. Bacteriochlorophyll a was not detected by in vivo spectroscopy or by in vitro spectroscopy in strains CFPB-A9T and CFPB-A5. Isolation of genomic DNA was carried out according to the method of Pitcher et al. (1989). The DNA base composition was determined by HPLC after enzymic digestion of DNA to deoxyribonucleosides (Katayama-Fujimura et al., 1984). A DNA-GC kit (Yamasa Shoyu, Tokyo, Japan) was used as a quantitative standard. The DNA G+C contents of the two strains, CFPB-A9T and CFPB-A5, seem to be substantially different from those of J. helgolandensis analysed by Wagner-Döbler et al. (2003) (Table 1). DNA–DNA hybridization experiments were performed in microdilution wells using a fluorometric binding method (Ezaki et al., 1988). The experiments showed a high level of DNA–DNA relatedness (99·2 %) between strains CFPB-A9T and CFPB-A5, and low levels of relatedness between J. helgolandensis and CFPB-A9T (20·5 %) and between J. helgolandensis and CFPB-A5 (19·1 %).
Quinones were extracted with chloroform/methanol (2 : 1, v/v) from cells of strains CFPB-A9T and CFPB-A5 grown for 5 days in Marine Broth 2216 at 25 °C. The extract was purified by the method described by Hiraishi et al. (1996) and analysed using a Shimazu LC-10 HPLC system (Shimazu, Tokyo, Japan). Analysis of the respiratory quinone composition indicated that Q-10 predominated in both strains. Fatty acid profiles of CFPB-A9T and CFPB-A5, and of J. helgolandensis Hel 10T as a reference strain, were quantified and identified by comparison to a commercial database, the Sherlock Microbial Identification System (MIS) by Microbial ID (MIDI) using the manufacturer's protocols. Isolate identifications were made by comparison to the MIDI TSBA (version 4.0) microbial database as described by Urbance et al. (2001). Cells used for the fatty acid analysis were grown on Marine Agar 2216 at 25 °C for 48 h. Fatty acid profiles for CFPB-A9T, CFPB-A5 and J. helgolandensis Hel 10T were dominated by 18 : 17c (>54 %). The profiles of these three strains had minor contributions from 3-OH 10 : 0 (3–8 %), unknown 11.799 (2–7 %), 18 : 0 (2–9 %) and methyl 18 : 17c (2–9 %) fatty acids. The similarity in fatty acid profiles among CFPB-A9T, CFPB-A5 and J. helgolandensis Hel 10T supports the CFPB strains as belonging to the genus Jannaschia. Significant differences in major (>10 % of total recovered fatty acids) or in minor (1–10 %) fatty acids were not observed between CFPB-A9T and CFPB-A5. However, cyclo 19 : 07c fatty acids were found in J. helgolandensis Hel 10T (17·7 %) but not in the two CFPB strains. Fatty acid profiles for the strains are available as supplementary material in IJSEM Online. In the case of J. helgolandensis Hel 10T, fatty acids 12 : 1, 17 : 0 and 20 : 0 were not detected by the Microbial ID system, whereas they had been detected in this strain by the analysis of Wagner-Döbler et al. (2003) using the method reported previously by Labrenz et al. (1998).
Bacterial genomic DNA was extracted according to the method described above. Sequences of the near-complete 16S rRNA gene were PCR-amplified using the 27F primer and the 1492R primer according to the method of Adachi et al. (2001). Completed amplifications were purified and quantified according to the method decribed by Adachi et al. (1996). PCR products were deprimerized using a GeneClean III Kit according to the manufacturer's recommendations (Bio101). The purified products were sequenced directly using a BigDye Terminator Cycle Sequencing FS Ready Reaction Kit (PE Biosystems), with bacterial universal 27F primer, and primers EUB338F, EUB338R, BAC514F, BAC514R, BAC785R, BAC1059F, BAC1059R, BAC1375F, BAC1375R and 1492R described previously (Adachi et al., 2001) and a newly designed primer, BAC785F (5'-GGATTAGATACGCTGGTAGTC-3'). The number in each primer name shows the corresponding position in the Escherichia coli 16S rRNA gene. DNA sequences were read directly to a computer using ABI PRISM 310 Genetic Analyser (PE Biosystems). Almost the entire 16S rRNA gene sequences were aligned to various bacterial 16S rRNA gene sequences obtained from the EMBL, GenBank and DDBJ databases using the software CLUSTAL W (version 1.6; EMBL). Distances were inferred from sequences using the one-parameter model (Jukes & Cantor, 1969). Branch lengths of phylogenetic trees were evaluated using the neighbour-joining method (Saitou & Nei, 1987) using CLUSTAL W and maximum-likelihood methods using DnaML, within the PHYLIP package (Felsenstein, 1995). Bootstrap analyses of 1000 replicates were carried out. Phylogenetic inferences were based on analysis of nearly complete 16S rRNA gene sequences of strains CFPB-A9T and CFPB-A5 (E. coli positions 49–1450). The 16S rRNA gene sequences of strains CFPB-A9T and CFPB-A5 were nearly identical (99·7 % similarity). The high similarity suggests that CFPB-A9T belongs to the same species as CFPB-A5. This was supported by the similarity in the DNA G+C contents of the two strains as well as the high level of DNA–DNA relatedness of these two strains, described above. Phylogenetic analyses revealed that the strains were members of the -Proteobacteria and were associated with the Roseobacter–Sulfitobacter–Silicibacter group described by Wagner-Döbler et al. (2003) (=Roseobacter group reported by González et al., 2000). Their nearest phylogenetic neighbour was J. helgolandensis Hel 10T (95·9 % sequence similarity). This similarity value (<97 %), the difference in their G+C contents and the low level of DNA–DNA relatedness between the CFPB strains and J. helgolandensis suggest that the CFPB strains represent a species different from J. helgolandensis. A phylogenetic tree of 16S rRNA gene relationships, displaying the positions of strains CFPB-A9T and CFPB-A5 relative to their neighbours, is shown in Fig. 2. Phylogeny shows that the CFPB strains always grouped with J. helgolandensis when different ingroups were included in the phylogenetic analysis with the neighbour-joining method (Fig. 2). The topology of the tree was confirmed using maximum-likelihood analyses (data not shown). These topologies were supported by high bootstrap values (98 %). These results suggest that the new strains belong to a novel species of the genus Jannaschia.
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Description of Jannaschia cystaugens sp. nov.
Jannaschia cystaugens [cyst.au'gens. Gr. n. cystis cyst; L. part. adj. augens promoting; N.L. part. adj. cystaugens promoting cyst (formation)].
Cells are Gram-negative, non-spore-forming, strictly aerobic and heterotrophic. Motile, irregular rods, 1·5–2·0 µm long and 0·5–0·8 µm wide. White inclusion bodies are sometimes observed. Oxidase-positive. Catalase-positive. Genomic DNA G+C content is 59·1–59·2 mol% (as determined by HPLC). Growth is typically observed after 5 days on Marine Agar 2216 plates, when incubated at 25 °C. Colonies are circular and convex with a cream-coloured margin and a raised, dark-brown centre. Older colonies become brown. The temperature range for growth is 5–30 °C, with an optimum of 25–30 °C. The pH range for growth is 7·0–9·0, with an optimum of pH 7·0. Growth is observed with 2–7 % (w/v) sea salts. The isoprenoid quinone type is Q-10. Primary cellular fatty acid is 18 : 17c. Cyclo 19 : 0 is not observed. Hydrolysis of gelatin, starch, urea, aesculin and p-nitrophenol-
-D-galactopyranoside is not observed. Does not reduce nitrate to nitrite. Growth occurs on D-glucose, glycerol, mannitol, sorbitol, starch, D-arabitol and gluconate. Isolated from sea-water samples obtained at a depth of 5 m in Hiroshima Bay, Japan. As well as the type strain, a reference strain (CFPB-A5=LMG 22016=NBRC 100363) is available.
The type strain is CFPB-A9T (=LMG 22015T=NBRC 100362T). Its G+C content is 59·1 mol%.
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ACKNOWLEDGEMENTS |
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D. R. Arahal, M. C. Macian, E. Garay, and M. J. Pujalte Thalassobius mediterraneus gen. nov., sp. nov., and reclassification of Ruegeria gelatinovorans as Thalassobius gelatinovorus comb. nov. Int J Syst Evol Microbiol, November 1, 2005; 55(6): 2371 - 2376. [Abstract] [Full Text] [PDF]
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M. J. Pujalte, M. C. Macian, D. R. Arahal, and E. Garay Thalassobacter stenotrophicus Macian et al. 2005 is a later synonym of Jannaschia cystaugens Adachi et al. 2004, with emended description of the genus Thalassobacter Int J Syst Evol Microbiol, September 1, 2005; 55(5): 1959 - 1963. [Abstract] [Full Text] [PDF]
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M. C. Macian, D. R. Arahal, E. Garay, W. Ludwig, K. H. Schleifer, and M. J. Pujalte Jannaschia rubra sp. nov., a red-pigmented bacterium isolated from sea water Int J Syst Evol Microbiol, March 1, 2005; 55(2): 649 - 653. [Abstract] [Full Text] [PDF]
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