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1 Laboratoire de Microbiologie, IMEP, Faculté des Sciences et Techniques de Saint Jérôme, 13397 Marseille cedex 20, France
2 Laboratoire de Biochimie et Biophysique des Systèmes Intégrés, DBMS/BBSI, CEA Grenoble, 38054 Grenoble, France
3 Division of Environmental and Applied Biology, Biological Sciences Institute, University of Dundee, Dundee DD1 4HN, UK
4 Laboratoire d'Ecologie Moléculaire-Microbiologie, IBEAS, BP 1155, Université de Pau, F 64013 Pau cedex, France
Correspondence
Pierre Caumette
pierre.caumette{at}univ-pau.fr
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ABSTRACT |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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), Rhodocista (Kawasaki et al., 1992; Favinger et al., 1989), Rhodospira (Pfennig et al., 1997) and Roseospirillum (Glaeser & Overmann, 1999). Among the purple sulfur bacteria, spiral-shaped bacteria are present in the Chromatiaceae (Thiospirillum) and the Ectothiorhodospiraceae as exemplified by the genera Ectothiorhodospira, Halorhodospira and Thiorhodospira (Imhoff & Süling, 1996; Bryantseva et al., 1999).
The majority of these bacteria require salt for optimal growth except for members of the genera Rhodospirillum, Phaeospirillum, Rhodocista and Thiospirillum. The salt-requiring bacteria have been isolated from coastal marine environments or inland salt lakes. Several have been isolated from hypersaline environments and described as moderately halophilic bacteria belonging to the genera Rhodovibrio, Rhodothalassium, Roseospira and Ectothiorhodospira. Only a few strains have been described as extreme halophiles and have been included in a single genus, Halorhodospira. Among all these spiral-shaped phototrophic moderate or extreme halophilic bacteria, a number have been isolated from sediment layers or deposits in hypersaline ponds or salt flats in evaporitic coastal environments. Within the purple non-sulfur bacteria, Rhodospirillum salexigens (Drews, 1981), later renamed Rhodothalassium salexigens (Imhoff et al., 1998), was isolated from hypersaline evaporated pools on the Oregon coast, USA, and Rhodospirillum salinarum (Nissen & Dundas, 1984), later renamed Rhodovibrio salinarum (Imhoff et al., 1998), was isolated from a Portuguese saltern. Similarly, among the purple sulfur bacteria Ectothiorhodospira mobilis (Trüper, 1968) was isolated from evaporitic salt flats in the Galapagos Islands. Other moderately to extremely halophilic purple sulfur or non-sulfur bacteria have been isolated from inland salt lakes or the Dead Sea.
During our investigation of microbial mats that develop in some lagoons within commercial salterns in the Rhône Delta (France), we observed a purple layer composed mainly of spiral-shaped bacteria below a thin gypsum crust. A number of strains were isolated and characterized. According to phenotypic and phylogenetic features, strain SG 3105 was related to Rhodovibrio sodomensis which was originally isolated by Mack et al. (1993) from the Dead Sea. The other isolated strains, SG 3301T, SG 3302 and SG 3304, were also characterized. According to physiological and phylogenetic features these strains are closely related to the genus Halorhodospira that contains extreme halophilic species isolated from inland salt lakes or the Dead Sea (Imhoff et al., 1998). However, none of the strains could be related to any currently described species of this genus. They are described in this paper together with Rhodovibrio sodomensis strain SG 3105 which was isolated from the same layer using the same growth medium. Strains SG 3301T, SG 3302 and SG 3304 represent a new species within the genus Halorhodospira for which we propose the name Halorhodospira neutriphila sp. nov. Strain SG 3301T (=DSM 15116T) is the type strain of the species.
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METHODS |
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of total salinity. From October to June lower salinities (240–280 ) occur. During the summer months (June to September) the salinity increases up to 320 , resulting in the deposition of halite; during this period, the microbial mats disappeared. The strains were isolated from samples collected when the microbial mats were fully developed in May to June.
Media, isolation and culture conditions.
The strains were isolated from enrichment cultures of red-layer samples. The enrichment medium was prepared according to Pfennig & Trüper (1992). It contained (l-1 distilled water): KH2PO4, 1 g; CaCl2.2H2O, 0·05 g; NH4Cl, 0·5 g; NaCl, 100 g; MgCl2.6H2O, 2 g; MgSO4.7H2O, 1 g; NaHCO3, 2 g; Na2S.9H2O, 0·75 g; vitamin solution V7, 1 ml; trace element solution SL12, 1 ml. The pH was adjusted to pH 7·2–7·4. For enrichments and for better growth of pure cultures, the growth medium was supplemented with acetate (2 mM), succinate (1 mM) and yeast extract (0·5 g l-1).
Pure cultures were obtained after isolation from a deep-agar shake dilution series prepared according to the method of Pfennig & Trüper (1992) and incubated at 30 °C and at a light intensity of 500 lux from a tungsten lamp (16 h light, 8 h dark). Purity of cultures was checked by both microscopic observation and growth tests in deep agar AC medium (Difco) supplemented with NaCl and thiosulfate (final concentrations 10 and 0·05 %, w/v, respectively) and incubated in the dark. Pure cultures in liquid medium were stored in 60 ml screw cap bottles at 4 °C in the dark.
Microscopy.
Microscopic observations and photomicrographs were made with a Zeiss photomicroscope according to the method of Pfennig & Wagener (1986). Flagella were observed by transmission electron microscopy (TEM) after negative staining with 1 % (w/v) tungstic acid neutralized to pH 7·2 (JEOL 1200 EX electron microscope). The fine structure of the cells was studied by TEM after fixation of a cell pellet with osmic acid and ultrathin sectioning of the cells according to Reynolds (1963).
Pigment analysis and DNA base composition.
Absorption spectra of living cells were measured with a Kontron spectrophotometer (UVIKON 860) after suspension of a cell pellet in sucrose solution (Pfennig & Trüper, 1992). Carotenoids were extracted and separated by TLC according to the method described by Eichler & Pfennig (1986). They were determined by comparison with several standards.
The G+C content of the DNA was determined by HPLC as described by Mesbah et al. (1989), using bacteriophage 
DNA as the standard.
16S rDNA sequence.
Isolation of genomic DNA, amplification of 16S rDNA by PCR, sequencing and phylogenetic analysis were all carried out as described previously (Mouné et al., 1999, 2000). The accession numbers of all 16S rDNA sequences used in this study are given in Fig. 4.
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Micro-aerophilic growth was tested in uniformly inoculated deep agar tubes open to air and incubated in the dark at 25 °C (Kämpf & Pfennig, 1980). Vitamin requirement and capacity for assimilatory sulfate reduction were tested in 60 ml screw cap bottles by growth tests through four consecutive transfers in synthetic liquid media free of vitamins and yeast extract or sulfide, respectively.
Nitrogen sources were tested in 60 ml aluminium cap sealed bottles with gas-impermeable butyl rubber septum stoppers filled one-third with liquid medium without nitrogen sources and supplemented with 10 mM acetate, and two-thirds with argon as gas phase. The tested nitrogen sources (ammonia, nitrate, organic nitrogen in cysteine, serine and glutamate) were added prior to inoculation. For nitrogen fixation, the gas phase was replaced by N2 gas (100 kPa). Growth was tested through four consecutive transfers under the same conditions.
Hydrogen utilization was tested by the same method in liquid medium without electron donors with only 0·5 mM Na2S.9H2O as sulfur source and with H2/CO2 (80 : 20, v/v; 100 kPa) as the gas phase. The presence of hydrogenase was tested according to the method of Trüper (1968).
Growth on sulfide, sulfide+CO2 and on sulfide+acetate was tested in 1 l cultures grown in synthetic liquid medium for 15 days. Growth was measured periodically by OD650 (Spectronic 20; Bausch and Lomb). Sulfide, sulfur and sulfate concentrations were determined according to the methods of Cline (1969), Stal et al. (1984) and Tabatabaï (1974), respectively.
The presence of catalase was determined by adding a few drops of 3 % (v/v) H2O2 to 2 ml of a dense cell suspension.
Determination of compatible solutes by 13C-NMR spectroscopy.
Isolate SG 3301T was grown as an 8 l batch culture in synthetic growth medium supplemented with 2 mM acetate and 1 mM succinate plus 15 % (w/v) NaCl but without yeast extract. Cultures were incubated at room temperature (25 °C) in the light and continuously sparged with oxygen-free nitrogen to maintain anaerobic conditions. Mid-exponential phase (OD650=0·4) cultures were harvested, extracted and analysed for compatible solutes by natural abundance NMR according to the methods of Welsh & Herbert (1994).
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RESULTS |
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; Caumette et al., 1988, 1991, 1994). These mats are present for most of the year and are fully developed in spring and summer, from May to September. The thickest mats (10–20 mm thick) were observed at the sediment surface of a series of lagoons below a 2–3 cm thick gypsum crust. In these lagoons the salinity of the water column (20–40 cm depth) ranged from 130 to 200 . These microbial mats consisted principally of a green layer of cyanobacteria overlying a purple layer of phototrophic sulfur bacteria belonging to the family Chromatiaceae (Caumette et al., 1988, 1991, 1994).
In contrast, in other lagoons with higher water salinities ranging from 200 to 320 , the gypsum crust at the sediment surface was thinner (2–5 mm thick) and it was periodically covered by halite crystals when the salinity increased above 300 . In these lagoons, from May to June, a laminated mat developed at the sediment surface, below the gypsum crust. The sediment was composed of a closed anoxic system containing high amounts of AVS (total acid-volatile sulfide) up to 20–40 mmol kg-1 (Caumette et al., 1991, 1994). When the salinity increased up to 300 in July, the mat decreased gradually and then disappeared by the end of the summer. This mat consisted mainly of a green layer of cyanobacteria (Phormidium-like). Below this layer, a red layer occurred. Microscopic observations revealed the sole presence of actively motile spirilloid cells that formed the red layers (Fig. 1). Free sulfur globules were also present and distributed in the entire layer. From red layer samples, enrichment cultures of spirilloid purple sulfur bacteria were obtained. Several strains were then isolated in the same synthetic growth medium with 10 % (w/v) NaCl. Four strains (SG 3301T, SG 3302, SG 3304 and SG 3105) were isolated, maintained in pure culture and characterized.
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a, b and c). In the presence of acetate or succinate, some larger non-curved cells containing reserve material (PHB) occurred with a width of 1·4–1·6 µm. The morphology of strain SG 3105 consisted of motile spirilloid cells of 2–4 µm length and 0·5–0·6 µm width. In contrast to the other strains, sulfur globules were never observed in the growth medium of strain SG 3105 (Fig. 2d). The cells of all strains divided by binary fission.
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a, b), cells of strains SG3301T and SG 3304, and also SG 3302 (not shown), contained similar pigments: BChl a with absorption maxima at 376, 589, 786–787 and 883–884 nm; carotenoids of the normal spirilloxanthin series with absorption maxima at 486–488, 519–520 and 556 nm. Spirilloxanthin was the dominant carotenoid present as determined by TLC. The colour of the cell suspension of strain SG 3105 was red to brown-red. Absorption spectra of whole cells (Fig. 3c) showed maxima at 379, 591, 804 and 857 nm typical for BChl a containing cells, and at 486, 516 and a shoulder at 545 nm, indicative of the presence of carotenoids of the normal spirilloxanthin series. The absorption maximum at 486 nm indicated the presence of rhodopin as a major carotenoid pigment and this was confirmed by TLC.
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). Three strains, SG 3301T, SG 3302 and SG 3304, were able to weakly use sulfide and sulfur. However, with these compounds as electron donors and CO2 as sole carbon source, the growth of the three isolates was very poor. In contrast all three strains showed good growth with a limited range of organic substrates as electron donors and carbon sources: pyruvate, fumarate, succinate, acetate and for certain strains, propionate and yeast extract. Strain SG 3105 is an obligate photo-organotroph and able to use a large variety of organic substrates (Table 1).
Effect of salt on the growth of the four strains.
The four strains SG 3301T, SG 3302, SG 3304 and SG 3105 grew at NaCl concentrations ranging from 6–8 % to 25–30 % (w/v) NaCl. The optima for all strains ranged from 9 to 12 % (w/v) NaCl. These results demonstrate a good adaptation of the strains to their environment where the total salinity of 240–320 corresponds approximately to 17–25 % (w/v) NaCl in the overlying water.
The requirement for Mg2+ was tested for the four strains, between 0 and 200 mM Mg2+. Strains SG 3301T, SG 3302 and SG 3304 required a minimum of 0·5 mM with optimal growth recorded at 50, 100 and 20 mM respectively. Strain SG 3105 required at least 7·5 mM for growth with an optimum at 100 mM. None of the isolates showed improved growth at Mg2+ concentrations above the optimum concentrations for growth.
Genetic properties and 16S rDNA sequences of the isolated strains.
The G+C of the DNA of strains SG 3301T, SG 3304 and SG 3105 was 74·5, 74·1 and 69·2 mol%, respectively.
The phylogenetic trees obtained from the comparison of 16S rDNA sequences are presented in Fig. 4(a, b). The sequence of Fig. 4(a) shows the phylogenetic tree obtained for strain SG 3105 and the closest sequences. According to the homologies, this strain is closely related to the species Rhodovibrio sodomensis (98·8 % similarity). Fig. 4(b) shows the phylogenetic tree obtained for the sequences of strains SG 3301T and SG 3304 among the closest sequences. These two strains are identical (100 % homology) among the genus Halorhodospira and close to Halorhodospira halophila DSM 244T (94·6 % similarity) which is the type species of the genus. The other two strains of the species (BN 9624 and BN 9630) are less closely related to our strain, with percentage similarities of 91·4 and 90·7 %, respectively. These percentage similarities indicate that strains SG 3301T and SG 3304 are sufficiently distant from H. halophila to be considered as representatives of a new species.
Additional characteristics of strains SG 3301T and SG 3304
Electron microscopy.
Fig. 5(a, b) shows electron micrographs of whole cells after negative staining (Fig. 5a) and a thin section of the cells of strain SG 3301T (Fig. 5b). The cells are polarly flagellated with a tuft of a few flagella. Thin sections of the cells revealed the presence of an intracellular membrane system comprising stacks of lamellar membranes.
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Cysteine served as sulfur source in the absence of sulfide. With sulfate as sole sulfur source, growth did not occur, indicating the absence of sulfate reduction.
Micro-aerophilic growth.
Growth of strain SG 3301T and SG 3304 was very poor or absent under micro-aerophilic conditions in the dark. Catalase was positive.
pH, light.
Strains SG 3301T and SG 3304 grew in media with a pH between 6 and 8·5. The optimum pH was 6·8–7·0 for both strains. Growth at different light intensities was determined between 25 and 5000 lux using a tungsten lamp light source. For both isolates growth was very slow at 25 lux. Optimal light intensity was recorded at 5000 lux for both strains with growth rates of 0·034 h-1 for strain SG3301 and 0·01 h-1 for strain SG 3304 under optimal conditions.
H2 and vitamin requirements.
Both strains SG 3301T and SG 3304 were unable to grow with H2 as sole electron donor. In addition, hydrogenase activity was tested and the result was negative for both strains.
Both strains were able to grow in synthetic growth medium in the absence of vitamins or yeast extract after five consecutive transfers, indicating that neither isolate had a vitamin requirement.
Sulfide tolerance and utilization of sulfur compounds as electron donors.
Strains SG 3301T and SG 3304 were able to grow with up to 5·5–6 mM sulfide in the synthetic growth medium. The optimum was 1–3 mM for both strains. For strain SG 3301T, with optimum sulfide, in the presence of CO2 as sole carbon source, growth was always very poor, although sulfide and the produced sulfur were completely oxidized to sulfate (Fig. 6a). In contrast with acetate as electron donor and carbon source, growth was always very good and the equivalent amount of sulfide and produced sulfur were also completely oxidized to sulfate (Fig. 6b). Sulfide could therefore be considered as a good electron donor for this strain, with or without an organic substrate, even though growth with sulfide and CO2 alone was very poor. This observation indicates that CO2 alone only supported limited growth of strain SG 3301T, as shown in Table 2. Maximal growth was obtained with sulfide, acetate and CO2 as substrates in the growth medium.
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DISCUSSION |
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. All the isolated strains grew between 6–8 and 25–30 % (w/v) NaCl in the synthetic growth medium with optima at 9–12 % (w/v) NaCl. Thus all strains can be considered as strictly halophilic to extremely halophilic bacteria (Caumette et al., 1999). Among these strains, the purple non-sulfur bacterium strain SG 3105 showed characteristics of the genus Rhodovibrio (Imhoff et al., 1998) and was more closely related to Rhodovibrio sodomensis on a physiological and phylogenetical basis, rather than to Rhodovibrio salinarum. This latter organism has been isolated from marine salterns (Nissen & Dundas, 1984) like our strain. In contrast Rhodovibrio sodomensis was first isolated from a hypersaline pond close to the Dead Sea (Mack et al., 1993). Thus our strain represents the first member of this species isolated from a marine saltern.
In this study, the three other isolated spirilloid strains (SG 3301T, SG 3302 and SG 3304) deposited sulfur globules extracellularly when grown with sulfide as electron donor. Morphologically, physiologically and phylogenetically they are fully included in the family Ectothiorhodospiraceae. This family is composed of three genera: Ectothiorhodospira, Halorhodospira and Thiorhodospira (Imhoff & Süling, 1996; Bryantseva et al., 1999). Our three isolated strains were more closely related to the genus Halorhodospira according to the phylogenetic tree based on comparison of 16S rDNA sequences. The genus Halorhodospira comprises the most halophilic and alkaliphilic representatives of the Ectothiorhodospiraceae, isolated from athalassohaline environments like the representative of the genus Thiorhodospira. In contrast, members of the genus Ectothiorhodospira have been isolated principally from coastal marine environments at neutral pH and at lower salinity, although some representatives are alkaliphilic and have been isolated from soda lakes (Imhoff & Süling, 1996). Therefore, our three strains which are extremely halophilic are the first members of the genus Halorhodospira isolated from marine salterns and living at neutral pH, thus showing that a moderate to extreme salt requirement is an important factor in bacterial taxonomy at the genus level, rather than pH.
All previous isolations of Halorhodospira spp. and Rhodovibrio sodomensis have been from enclosed hypersaline lakes. This study is the first to demonstrate their presence in a modified marine environment, indicating that they have a wider distribution than previously considered. The presence of these populations in the same depth horizon within the mats suggests that both populations are living in same conditions and possible interactions may be occurring. Evidence to support this conclusion is the ability of the purple sulfur Halorhodospira isolates to preferentially use low-molecular-mass organic substrates for growth rather than reduced sulfur compounds. This characteristic is more typical for the photoheterotrophic growth of Rhodovibrio sodomensis.
The salinity range for growth of the strains indicates that all these isolates are well adapted to life in the hypersaline lagoons from which they were isolated. Data presented in this study show that strain SG 3301T when grown at supra-optimal salt concentrations (15 %, w/v, NaCl) in the absence of yeast extract synthesized glycine betaine and ectoine as compatible solutes. Semi-quantitative estimation of the relative amounts of the accumulated osmolytes indicate that glycine betaine was the major osmoticum synthesized by this isolate and ectoine was the minor component. These data are in agreement with those of Severin et al. (1992) who showed that Halorhodospira halochloris, Halorhodospira abdelmalekii and Halorhodospira halophila also synthesized glycine betaine and ectoine when subjected to salt stress. Strain SG 3301T grows more rapidly when yeast extract is added to the growth medium. Since yeast extract contains significant amounts of glycine betaine (Dulaney et al., 1968) this suggests that strain SG 3301T may possess a functional glycine betaine uptake system. In hypersaline lagoons glycine betaine may account for >20 % of the total nitrogen present in the mats (King, 1988). Thus, from an ecological viewpoint the ability of an organism to accumulate a compatible solute such as glycine betaine would be advantageous since it is energetically more favourable than synthesis.
Among the Halorhodospira species, our strains (SG 3301T and SG 3304) are related to Halorhodospira halophila according to the rDNA sequence. However, the degree of similarity (94·6 % similarity) is not sufficiently high to include these isolates within the species Halorhodospira halophila. Physiologically, strain SG 3301T has several characteristics close to the Halorhodospira halophila type strain (DSM 244T, Table 3). Both strains contain BChl a and spirilloxanthin as the major carotenoid and have higher G+C contents in their DNA, whereas the two other Halorhodospira species (Halorhodospira abdelmalekii and Halorhodospira halochloris) are different with BChl b and rhodopin as the major photopigments, and a lower G+C content in their DNA. However, Halorhodospira strain SG 3301T differs from Halorhodospira halophila by its flagella pattern with one polar tuft rather than bipolar flagellation for Halorhodospira halophila and also for other Halorhodospira (Table 3). Their DNA G+C content ratios are also different with 74·5 mol% for strain SG 3301T and 67·5–69·7 mol% for Halorhodospira halophila. There are also additional physiological differences between both micro-organisms. Halorhodospira halophila is able to use thiosulfate and malate as electron donor whereas Halorhodospira strain SG 3301T, is unable to use these substrates and grows poorly on all other sulfur compounds, which is not an usual characteristic of the purple sulfur bacteria. The most important difference between strain SG 3301T and Halorhodospira halophila is the optimal pH for growth. All Halorhodospira species are alkaliphilic with pH optima between 8·0 and 9·0. In contrast, strain SG 3301T grows optimally at neutral pH (6·8–7·0) like other isolated strains (SG 3302 and SG 3304). The three isolated strains are all very similar. According to their morphological, physiological and genetic differences with the described species in the genus Halorhodospira, it is justifiable to consider the three strains as members of a new species for which the name Halorhodospira neutriphila sp. nov. is proposed with respect to their optimal growth at neutral pH. Strain SG 3301T is proposed as the type strain of this new species.
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, but with the following additional features: motile by polar tuft of flagella; growth is dependent on saline conditions and neutral or alkaline pH. Halorhodospira species are found in hypersaline and extremely saline environments with neutral to extremely alkaline pH that contain sulfide and that are exposed to light, such as salterns, salt flats, salt lakes and soda lakes. The G+C content of the DNA is 50·5–74·5 mol%.
Description of Halorhodospira neutriphila sp. nov.
Halorhodospira neutriphila (neu.tri.phi'la. L. adj. neutralis neutral; Gr. adj. philos liking, preferring; N.L. adj. neutriphila preferring neutral pH).
Cells are curved rods, 1–1·2 µm wide and 2–5 µm long. Multiplication is by binary fission. Gram-negative. Cells are motile by a polar tuft of flagella. Colour of cell suspension is pinkish-red. Photosynthetic membrane system, present as lamellar stacks, contains BChl a and spirilloxanthin as the major carotenoid. Electron donors for photoautotrophic growth are sulfide and sulfur. Globules of elemental sulfur are present outside the cells. Photoautotrophic growth is poor. In the presence of sulfide and CO2, acetate, pyruvate, fumarate, succinate and yeast extract are photoassimilated. Propionate can be used by some strains. Not capable of chemolithotrophic or chemo-organotrophic growth. Not capable of assimilatory sulfate reduction. N2 and NH4 serve as nitrogen sources. Cysteine is used as sulfur source. No vitamins are required. Optimal pH, 6·8–7·0; pH range for growth, 6·0–8·5; optimal temperature, 30–35 °C; NaCl range is between 6–8 and 25–30 % (w/v) NaCl; optimal concentration at 9–12 % (w/v) NaCl. G+C content of DNA is 74·1–74·5 mol% (HPLC). Habitat is anoxic mud, sediments and microbial mats exposed to light in hypersaline to extreme saline environments, such as coastal salterns with salt concentrations of approximately 20–30 % (w/v). Type strain is SG 3301T (=DSM 15116T) isolated from a benthic microbial mat in a commercial saltern, Salin-de-Giraud (Camargue, France). The 16S rDNA sequence has been deposited in the EMBL database under the accession number AJ318525. The second strain, SG3304, has also been deposited in the DSMZ as DSM 15115 and its 16S rDNA sequence accession number is AJ318526.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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