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1 GBF – Gesellschaft für Biotechnologische Forschung, D-38124 Braunschweig, Germany
2 Technical University of Braunschweig, D-38106 Braunschweig, Germany
3 University of Göttingen, D-37077 Göttingen, Germany
4 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen, D-38124 Braunschweig, Germany
Correspondence
Irene Wagner-Döbler
iwd{at}gbf.de
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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7c, 18 : 0, 16 : 17c, 16 : 0, 3-OH 10 : 0, 3-OH 12 : 1 (or 3-oxo 12 : 0) and traces of an 18 : 2 fatty acid. Among the hydroxylated fatty acids only 3-OH 12 : 1 (or 3-oxo 12 : 0) appears to be amide linked, whereas 3-OH 10 : 0 appears to be ester linked. The minor fatty acid components (between 1 and 7 %) allow three subgroups to be distinguished in the Sulfitobacter/Staleya clade, placing HEL-45T into a separate lineage characterized by the presence of 3-OH 12 : 1 (or 3-oxo 12 : 0) and both ester- and amide-linked 16 : 17c phospholipids. HEL-45T produces indole and derivatives thereof, several cyclic dipeptides and thryptanthrin. Phylogenetic analysis of 16S rRNA gene sequences and chemotaxonomic data support the description of a new genus and species, to include Oceanibulbus indolifex gen. nov., sp. nov., with the type strain HEL-45T (=DSM 14862T=NCIMB 13983T).
Published online ahead of print on 5 March 2004 as DOI 10.1099/ijs.0.02850-0.
The EMBL/GenBank/DDBJ accession number for the 16S rRNA gene sequence of HEL-45T is AJ550939.
Present address: Bayer AG, D-51368 Leverkusen, Germany. 
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), a cluster of genera phylogenetically related to the genus Roseobacter within the ‘Alphaproteobacteria’. These bacteria have attracted interest over the last few years because they are the closest cultivated relatives of the second most abundant uncultivated lineage in the marine picoplankton, the SAR83 cluster (Giovannoni & Rappé, 2000; Rappé et al., 2000).
Cultivated representatives of the Roseobacter lineage display interesting physiological capabilities that may be of great importance for the marine ecosystem, e.g. aerobic anoxygenic photosynthesis (Yurkov & Beatty, 1998a), the turnover of the greenhouse gas dimethylsulfoniopropionate (DMSP) (Zubkov et al., 2001) or the production of sodium-channel blocking toxins, which has been found in Sulfitobacter strains from toxic dinoflagellates (Vasquez et al., 2001, 2002).
Of the Roseobacter clade strains isolated from the Helgoland water sample, one group of strains (HEL-10T, HEL-43, HEL-26) was only distantly related to any of the described genera in this group and has recently been described as Jannaschia helgolandensis (Wagner-Döbler et al., 2003). Here, we report the description of strain HEL-45T, which is phylogenetically related to both Sulfitobacter and Staleya and produces a number of interesting secondary metabolites, which were analysed by Kampen (2001), Schröder (2002) and Lurtz et al. (2002) (Fig. 1). These authors identified indole and several indole derivatives, e.g. indole-3-carboxylic-thiomethylester, 3-indole-carbaldehyde and 3,3-bis-(indol-3-yl)-propane-1,2-diol. Moreover, bioactive compounds were found. Three cyclic dipeptides were identified, namely cyclo-(Leu,Pro), cyclo-(Phe,Pro) and cyclo-(Tyr,Pro), which are known to have weak antiviral, antibiotic and antitumour activity (Milne et al., 1998). In addition, tryptanthrin was found, which is known to have activity against some Gram-positive bacteria as well as fungi of the genera Trichophyton and Microsporum (Honda et al., 1979).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Culture conditions.
Strain HEL-45T was initially isolated from the so-called marine cytophaga medium (DSMZ medium 172). Routine culturing using a modified Luria–Bertani agar medium, containing additional sea salts (designated LBSS: 10·0 g tryptone, 5·0 g yeast extract, 10·0 g NaCl, 14·0 g sea salts, 15·0 g agar, in 1000 ml distilled water) was found to be more suitable. Working stocks of the isolate were preserved in glycerol. Storage was carried out by inoculating 5 ml LBSS broth with a loopful of cell material and shaking for 2–3 days at 30 °C. Aliquots of 1·5 ml of the suspension were centrifuged (7000 g, 5 min), and the supernatant was discarded. After resuspending the pellet in 500 µl fresh LBSS broth, 750 µl sterile glycerol (99·5 % w/v) was added and mixed. The suspension was then equilibrated on ice for 30 min, followed by freezing at –18 °C for 2 h and final storage at –70 °C. For reactivation, 50 µl of the suspension was recultivated by streaking on LBSS agar.
Determination of physiological characteristics.
A loopful of cell material of strain HEL-45T was taken from a fresh culture on solid LBSS medium. A suspension corresponding to McFarland standard 1 (OD550=0·25; bioMérieux) was prepared in 10 ml saline buffer supplemented with 2 % (w/v) sea salts (Sigma). The optical density was adjusted by addition of either buffer or cell material. One drop of this suspension was added to each of the test tubes or test plates. Incubation of the test samples was performed at 25 °C.
The temperature range for growth was tested in LBSS broth from 4 to 60 °C, and halotolerance was tested in medium devoid of NaCl with 0, 1, 3, 5, 7, 10, 13 or 15 % (w/v) sea salts added. The pH range for growth was determined in a range from 5·0 to 11·0 in steps of one pH unit. The pH value was adjusted by addition of either HCl or NaOH. All tests were set up in duplicate. Anaerobic growth was also tested on agar plates containing LBSS medium, incubated in an anaerobic jar.
The following physiological tests were carried out according to methods described by Gordon et al. (1973): catalase reaction, oxidase reaction, presence of urease, decomposition of Tween 80, starch hydrolysis and nitrite production.
Gelatin liquefaction was tested following the method of Gerhardt et al. (1981) in that plates of LBSS containing 0·4 % gelatin were incubated with strain HEL-45T for 7 and 14 days. Plates were then flooded with warm (55 °C) 0·5 M sulfuric acid, saturated with Na2SO4. A resulting clear circular zone around the colony indicated digestion of the gelatin. Hydrolysis of aesculin was tested in accordance with Lanyi (1987) in a medium consisting of 10·0 g Bacto-peptone, 1·0 g sodium citrate, 1·0 g aesculin and 0·05 g ferric citrate in 1000 ml water at pH 6·8–7·0.
Carbon utilization was tested in standard mineral base medium (Stanier et al., 1966) containing 0·2 % of the carbon source. A negative control without carbon source was also included. As no growth could be observed in any of these tests, they were repeated with the addition of three drops of sterile 0·1 % yeast extract to each of the test tubes. Even under these conditions, the negative control did not show any growth. The tests were examined for growth daily for up to 2 weeks until no further growth in the test tubes was observed. Carbon sources thus tested were: glucose, acetate, propionate, butyrate, pyruvate, DL-lactate, L-aspartate, asparagine, L-glutamate, L-proline, L-serine, DL-alanine, L(+)-ornithine, succinate and methanol. Physiological reactions were also tested using the substrate panel of the API 20 NE and API 50 CH systems (bioMérieux). Additional carbon sources covered by these systems were: D-arabinose, mannose, mannitol, N-acetylglucosamine, maltose, gluconate, caprate, adipate, malate, citrate, phenylacetate, glycerol, erythritol, L-arabinose, ribose, D-xylose, L-xylose, adonitol, methyl 
-xyloside, galactose, D-fructose, L-sorbose, rhamnose, dulcitol, inositol, sorbitol, methyl 
-D-mannoside, methyl -D-glucoside, amygdalin, arbutin, aesculin, salicin, cellobiose, lactose, melibiose, sucrose, trehalose, inulin, melezitose, D-raffinose, starch, glycogen, xylitol, -gentiobiose, D-turanose, D-lyxose, D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol, 2-ketogluconate and 5-ketogluconate.
Carbon sources that tested negatively but are not included in Table 1 (see Results and Discussion) owing to a lack of data for the phylogenetic relatives are: D-arabinose, maltose, caprate, phenylacetate, erythritol, L-arabinose, ribose, D-xylose, L-xylose, adonitol, methyl -xyloside, L-sorbose, dulcitol, inositol, tryptophan, methyl -D-mannoside, methyl -D-glucoside, amygdalin, arbutin, salicin, melibiose, trehalose, inulin, melezitose, D-raffinose, starch, glycogen, xylitol, -gentiobiose, D-turanose, D-lyxose, D-tagatose, D-fucose, L-arabitol, 2-ketogluconate and 5-ketogluconate.
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-galactosidase were additionally tested by reading and interpreting the corresponding API tests.
Microscopic investigations.
Primary morphological characterization was by light microscopy, including phase-contrast observations. The size and ultrastructure of the cells were determined by electron microscopy. Cell morphology was investigated using slides covered with 2 % (w/v) agar (dissolved in water). Transmission electron microscopic investigations were carried out as described by Rheims et al. (1999). Staining for poly--hydroxybutyrate was performed as follows. A heat-fixed film was prepared on a microscope slide from a drop of culture fluid. The slide was immersed in Sudan black B (0·3 % w/v in ethanol) for 5–15 min, drained and air-dried on blotting paper. The slide was then immersed in xylene and withdrawn several times, and then blotted dry. For counterstaining, the slide was immersed in an aqueous safranin solution (0·5 % w/v) for 5–10 s, rinsed with tap water and blotted dry. Examination was under the light microscope with and without phase-contrast optics. Poly--hydroxybutyrate inclusion bodies appear blue–black and the cytoplasmic parts of the organism appear pink (following counterstaining).
Chemotaxonomy.
Analysis of fatty acid methyl esters was performed with 20 mg freeze-dried biomass as described by Labrenz et al. (1998). Respiratory lipoquinones and polar lipids were extracted from 100 mg freeze-dried material using a two-stage extraction method and analysed as described by Tindall (1990a, b).
Determination of base composition of DNA.
Isolation of DNA (Cashion et al., 1977) and determination of the DNA G+C content (mol%) by HPLC (Mesbah et al., 1989) followed standard procedures.
DNA–DNA hybridization.
DNA–DNA relatedness studies were performed by the renaturation method (Escara & Hutton, 1980; Huß et al., 1983). Relatedness values were calculated according to the methods of Jahnke (1992).
Phylogenetic inferences.
Genomic DNA was extracted from bacterial cells and purified as described by Pukall et al. (1998). The primer pair 27f (5'-GAGTTTGATCCTGGCTCAG-3') and 1527r (5'-AGAAAGGAGGTGATCCAGCC-3') was used for amplification of the 16S rRNA gene (Lane, 1991). Amplification of 16S rRNA gene sequences by PCR was performed as described by Pukall et al. (1999). Analysis of the 16S rRNA gene sequence obtained from isolate HEL-45T followed the method described by Rainey et al. (1996) using the Taq DyeDeoxy Terminator cycle sequencing kit (Applied Biosystems) and an Applied Biosystems model 373A automated DNA sequencer. Sequences were aligned manually and compared to previously published sequences. These were stored in the DSMZ internal database consisting of more than 6000 16S rRNA gene sequence entries, including those from the Ribosomal Database Project (Maidak et al., 2001) and EMBL. Similarity values were transformed into genetic distance values that compensate for multiple substitutions at any given site in the sequence (Jukes & Cantor, 1969). The neighbour-joining method contained in the PHYLIP package (Felsenstein, 1993) and the algorithm of DeSoete (1983) were used in the construction of the phylogenetic dendrogram. All analyses were performed on a SUN SparcII workstation.
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RESULTS AND DISCUSSION |
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). A few individual cells under microscopic investigation had a bulbous end. Some cells were observed in stages resembling branching or budding. Strain HEL-45T could be shown to stain Gram-negatively by classical staining techniques as well as by cell lysis after the addition of 3 % (w/v) KOH. As judged by microscopic investigations, HEL-45T does not form spores. White inclusion bodies were often present, which were clearly not gas vesicles, as judged by transmission electronic investigations (Fig. 2, and further data not shown). These inclusion bodies stained black with Sudan black, suggesting they probably consist of poly--hydroxybutyrate. Active motility was not observed.
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Growth was poor at 8 °C and continued at up to 30 °C with an optimum temperature of 25–30 °C. The pH range tolerated for growth was 7·0–9·0 with an optimum at pH 7·0. Strain HEL-45T showed no growth in media devoid of salts. When only sodium chloride was added to the test medium, strain HEL-45T also failed to grow. Therefore, determination of halotolerance was carried out with the addition of commercially available sea salts. Growth started at a concentration of 1 % salts and continued up to 10 % with an optimum around 3–5 % (w/v).
The results of further physiological tests are summarized in Table 1
. Also included are some of the literature data for the closest phylogenetic relatives as judged by 16S rRNA gene sequence analysis. Further carbon sources that were tested but gave negative results are listed in Methods. Test results for hydrolysis of gelatin, starch, Tween 80, urea and aesculin were negative.
Phylogenetic inferences
Analysis of the nearly complete 16S rRNA gene sequence indicated that strain HEL-45T shared 97·4 % sequence similarity with the sequence of Sulfitobacter mediterraneus DSM 12244T. Similarity values determined for the other species of the genus Sulfitobacter and for Staleya guttiformis and Roseobacter litoralis ranged between 97·0 and 96·4 % (Fig. 3).
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), base pairs of HEL-45T were different from those of Sulfitobacter species or Staleya guttiformis. For those strains, the following combinations were found at the same positions: 132–230, A : U (all); 140–223, U : G (Sulfitobacter mediterraneus), U : A (others); 144–178, A : U (all); and 1356–1366, U : A (all). DNA–DNA relatedness determined by the spectrophotometric method revealed only a low value of 21·2 % between strains HEL-45T and Sulfitobacter mediterraneus DSM 12244T. The G+C content of the DNA for strain HEL-45T was determined to be 60·1 mol%.
Chemotaxonomic properties
Analysis of the respiratory quinone composition of strain HEL-45T, Sulfitobacter pontiacus DSM 10014T, Sulfitobacter brevis DSM 11443T, Sulfitobacter mediterraneus DSM 12244T and Staleya guttiformis DSM 11458T indicated that Q10 predominated in all strains. The presence of Q10 as the dominant respiratory quinone is a feature of many, but not all, members of the ‘Alphaproteobacteria’. Although Q10 is also found in Legionella species (‘Gammaproteobacteria’), it is not the sole, major component in these bacteria, making the presence of Q10 as the sole major respiratory quinone specific to members of the ‘Alphaproteobacteria’.
The polar lipid composition of all strains showed a high degree of similarity, with the phospholipids phosphatidyl glycerol, phosphatidyl choline and phosphatidyl ethanolamine all present. In addition, an aminolipid was also present. Diphosphatidyl glycerol was not universally present. The fatty acid composition of all strains gave patterns in which 18 : 17c predominated, but different groupings could be distinguished on the basis of the remaining fatty acids; these are listed in Table 2.
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, we have been able to confirm some degree of infrastructure within this group based on the polar lipid and fatty acid composition. We observed some differences in the relative percentages of the fatty acids compared to previous work, although small changes are to be expected in the relative composition owing to slight differences in conditions of cultivation, and should not be overemphasized when evaluating the data. Closer examination of the fatty acid composition revealed three major groups: (i) Sulfitobacter pontiacus DSM 10014T/Sulfitobacter brevis DSM 11443T, (ii) strain HEL-45T and (iii) Staleya guttiformis DSM 11458T/Sulfitobacter mediteraneus DSM 12244T. In particular, although all members of this group produced 3-OH 10 : 0, there were differences in the distribution of other 3-OH fatty acids. It should be noted that unambiguous proof is not presented here that the 3-OH 12 : 1 or 3-OH 14 : 1 are not 3-oxo derivatives, which are very difficult to distinguish on the basis of mass spectrometry alone. Sulfitobacter pontiacus DSM 10014T and Sulfitobacter brevis DSM 11443T produced 3-OH 12 : 0 and 3-OH 14 : 1 (or 3-oxo 14 : 0), whereas Staleya guttiformis DSM 11458T and Sulfitobacter mediteraneus DSM 12244T produced only 3-OH 14 : 1 (or 3-oxo 14 : 0) and strain HEL-45T produced 3-OH 12 : 1 (or 3-oxo 12 : 0). For the fatty acids identified here as 3-OH 12 : 1 (or 3-oxo 12 : 0), 3-OH 12 : 0 and 3-OH 14 : 1 (3-oxo 14 : 0), all appeared to be amide linked.
Although it may not be possible to determine with absolute certainty the branching order within the group defined by members of the genera Staleya–Sulfitobacter–strain HEL 45T based on the 16S rRNA gene sequences, it is sufficient that groups be clearly distinguished from one another (Tindall, 1994), there being a distinct and subtle difference between phyletic lineages and phyletic groups (Gilmour, 1940). It is particularly interesting that Sulfitobacter pontiacus DSM 10014T/Sulfitobacter brevis DSM 11443T, strain HEL-45 and Staleya guttiformis DSM 11458T/Sulfitobacter mediteraneus DSM 12244T form three distinct groups based on their chemical composition.
The data presented here are consistent with what has been reported previously in the literature, where the absolute branching order of taxa showing short internal branches cannot be determined unambiguously based on the 16S rRNA gene sequence data alone. Ludwig et al. (1998) proposed that in such cases the branches should be collapsed to give a ‘collapsed clade’. In such cases, the 16S rRNA gene sequence data can only give a polychotomy at best, which would suggest that this group of strains represents a single genus. However, the chemical composition clearly indicates that there is infrastructure within this group and may be used to define at least three subgroupings. These groupings appear to be no less significant than those defined by other genera in which the chemical composition, 16S rRNA gene sequences and biochemical/physiological data have been taken into consideration in this subgroup of the ‘Alphaproteobacteria’ (see Labrenz et al., 1998, 1999, 2000). It should be noted that the 16S rRNA gene sequence similarity between the strains is greater than 96 %, suggesting that the often used value of 95 % similarity for delineating genera would not take into account the chemical diversity of this group. In fact, using the value of 95 % similarity as a cut-off value would imply that all these species should be placed in the genus Roseobacter.
In the case of strain HEL-45T, we interpret the chemical composition of the cell as being indicative of the fact that this strain, which obviously represents a novel species, should also be placed in a new genus. The chemical heterogeneity evident within the genus Sulfitobacter, as currently defined, would justify transferring Sulfitobacter mediterraneus to the genus Staleya. However, the ability for aerobic anoxygenic photosynthesis has been found in Staleya and is a significant physiological trait that has to be weighed against the chemical composition of the cells (Yurkov & Beatty, 1998a, b). In the absence of additional information, and in view of the needs of the end users of bacterial systematics, we therefore refrain at present from transferring Sulfitobacter mediterraneus to the genus Staleya.
Description of Oceanibulbus gen. nov.
Oceanibulbus (O.ce.a.ni.bul'bus. L. n. oceanus the sea; L. n. bulbus onion; N.L. masc. n. Oceanibulbus onion-like bacterium from the sea).
Gram-negative, non-motile irregular rods with a tendency to form slightly swollen ends. On LBSS agar, the strain develops colonies within 3–5 days. They do not form spores. Bacteriochlorophyll a is not produced. Growth is poor at 15 °C and optimal at 25–30 °C. pH optimum for growth is 7·0–8·0. Strictly aerobic, non-fermentative heterotrophs. Inclusion bodies often present. In media devoid of salts or containing only sodium chloride, no growth is observed. Growth at 1–7 % (w/v) sea salts. They show a weakly positive reaction in tests for cytochrome oxidase and do not reduce nitrate to nitrite. The predominant respiratory quinone present is ubiquinone 10 (Q10). The major polar lipids are phosphatidyl glycerol, diphosphatidyl glycerol, phosphatidyl choline, phosphatidyl ethanolamine and an aminolipid. The fatty acids comprise 18 : 17c, 18 : 0, 16 : 17c, 16 : 0, 3-OH 10 : 0, 3-OH 12 : 1 (or 3-oxo 12 : 0) and traces of an 18 : 2 fatty acid. Among the hydroxylated fatty acids only 3-OH 12 : 1 (or 3-oxo 12 : 0) appears to be amide linked, whereas 3-OH 10 : 0 appears to be ester linked. The type species is Oceanibulbus indolifex.
Description of Oceanibulbus indolifex sp. nov.
Oceanibulbus indolifex (in.do'li.fex. N.L. masc. n. indolum indole; L. masc. suff. -fex from L. v. facio to make; N.L. masc. adj. indolifex making indole/the indole maker).
Displays the following properties in addition to those given in the genus description. Cells are variable in size (3–5 µm long, 1·8–2·5 µm wide). They have inclusion bodies that appear white in transmission electron microscopic sections and consist of poly--hydroxybutyrate. Catalase-positive and weakly oxidase-positive. The G+C content of the type strain is 60·1 mol%. Cells grown on LBSS develop small, whitish, shiny colonies within 3–5 days. Hydrolysis of gelatin, starch, Tween 80, urea and aesculin is not observed. Strains do not reduce nitrate to nitrite. Carbon source utilization in standard mineral base medium (Stanier et al., 1966) containing 0·2 % of the carbon source and 0·1 % yeast extract shows utilization of D-glucose, pyruvate, DL-lactate, serine, ornithine, alanine, asparagine, L-aspartate, L-glutamate, L-proline, succinate, mannitol, adipate, malate, citrate and glycerol. Chemotaxonomic properties and other characteristics are as for the genus.
The type strain, strain HEL-45T (=DSM 14862T=NCIMB 13983T), was originally obtained from a North Sea water sample from a depth of 10 m. The EMBL accession number of the 16S rRNA gene sequence is AJ550939.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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