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1 Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospect 60-let Octyabrya 7/2, 117811 Moscow, Russia
2 Environmental Biotechnology, Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
3 Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands
4 Institute of Microbiology and Biotechnology, Rheinische Friedrich-Wilhelms University, Bonn, Germany
Correspondence
Dimitry Yu. Sorokin
soroc{at}inmi.host.ru
;
D.Y.Sorokin{at}tudelft.nl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains ASO3-1T, AHT 6T and AHT 8 are EU296537–EU296539.
A supplementary table showing a comparison of cellular fatty acid profiles of extremely natronophilic sulfidogenic isolates from hypersaline soda lakes with low salt-tolerant alkaliphilic and high salt-tolerant halophilic members of the family Desulfohalobiaceae is available with the online version of this paper.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) and high energy yields of sulfur-dependent dissimilatory metabolism (Oren, 1999) could be the reasons for this phenomenon. Our investigation of the oxidative part of the sulfur cycle in soda lakes has resulted in the isolation and characterization of more than a hundred strains of chemolithoautotrophic sulfur-oxidizing gammaproteobacteria that are well adapted to extreme haloalkaline conditions (Sorokin & Kuenen, 2005; Sorokin et al., 2006). However, little is known about the reductive part of the sulfur cycle in soda lakes. So far, only two culturable groups of moderately salt-tolerant alkaliphilic sulfate-reducing bacteria (SRB) belonging to the Deltaproteobacteria (order Desulfovibrionales) have been found in soda lakes. The genus Desulfonatronovibrio includes a single species, while the genus Desulfonatronum contains three species. Both utilize acetate as a carbon source, but not as an electron donor. H2 is used as an electron donor, but autotrophy has been reported only for Desulfonatronum thiodismutans (Zhilina et al., 1997, 2005; Pikuta et al., 1998, 2003). Quantitative data on SRB activity in soda lakes are scarce. The data on stratified alkaline lakes from North America indicate a sharp decrease of activity at a salt content above 100 g l–1 (Kulp et al., 2006), while our data on shallow soda lakes from Central Asia demonstrate high rates of sulfate reduction under hypersaline conditions up to saturation (Sorokin et al., 2004; Foti et al., 2007, 2008). The latter data suggest the presence of an active, but yet uncultured, high salt-tolerant alkaliphilic SRB group(s) in hypersaline soda lakes. Such SRB are presently known only among neutrophilic representatives of the family Desulfohalobiaceae, including the genera Desulfohalobium (Ollivier et al., 1991) and Desulfovermiculus (Belyakova et al., 2006). Culture-independent studies of the SRB populations in soda lakes so far are limited to two studies. In Mono Lake in California, 16S rDNA targeting has successfully identified representatives of several groups of deltaproteobacterial SRB (Scholten et al., 2005). Similar studies with sediments from soda lakes of the Kulunda Steppe (Altai, Russia) targeting the dsrAB gene (encoding the key enzyme dissimilatory sulfite reductase) have demonstrated the presence of two major groups of deltaproteobacterial SRB: one in Desulfovibrionales, related to two culturable groups; and several lineages within the family Desulfobacteriaceae, which includes mostly species utilizing acetate as electron donor (Foti et al., 2007). This suggests the presence of important functional, but yet uncultured, groups of bacteria involved in the reductive part of the sulfur cycle in soda lakes. In the current paper we describe a novel group of obligately alkaliphilic SRB found in hypersaline soda lakes. The most striking feature of these SRB was the potential to grow chemolithoautotrophically by fermentation (dismutation) of sulfite and thiosulfate. They represent a novel genus within the family Desulfohalobiaceae, for which we propose the name Desulfonatronospira gen. nov.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Foti et al., 2007, 2008). Potential rates of sulfidogenesis from sulfate and thiosulfate at high-salt conditions were measured with a sample from the hypersaline soda lake Bitter-1 at the Kulunda Steppe (July 2007) in a sediment slurry experiment (water pH=10.53, alkalinity=2.95 M; total salt=18.2 %; sulfate=9.8 mM; free sulfide in the sediments=0.95–1.30 mM). For this, one part of sediment from the top 10 cm layer was mixed with two parts of the near-bottom water sediment, and incubated anaerobically in duplicate with various electron donors and acceptors at 28 °C. Samples (100 µl) were taken regularly with a syringe for sulfide analysis. The maximum rates of sulfidogenesis were calculated for the linear period of sulfide production.
Medium composition and growth experiments.
A mineral medium based on sodium carbonate buffer at pH 10 containing 2.3 M total Na+ was used for the enrichments (concentrations in g l–1): Na2CO3, 95; NaHCO3, 15; NaCl, 15; K2HPO4, 0.5. For pure culture studies, the soda content of the mineral base varied from 0.6 to 4 M total Na+. After sterilization, the medium was supplemented with 1 mM MgCl2, 1 ml l–1 trace metal solution (Pfennig & Lippert, 1966) and 0.1 mg l–1 filter-sterilized vitamin B12. Sulfite was used at a final concentration of 10 mM, thiosulfate and sulfate at a concentration of 20 mM. Other electron acceptors were used at 5 mM concentration. Electron donors were used at 10 mM concentration, except formate, which was used at a concentration of 50 mM. Routine cultivation was performed in 100 ml serum bottles that were closed with butyl rubber stoppers and contained 80 ml of culture medium. In the case of H2 as electron donor, the amount of medium was reduced to 50 ml. After the addition of the electron donor and electron acceptor, the cultures were made anoxic by several cycles of evacuation-flushing with argon or hydrogen. Sodium sulfide (1 mM) was used as a reducing agent. The cultures were incubated at 30 °C and were periodically checked for sulfide production. When the sulfide concentration exceeded 5–8 mM, the culture was transferred into new medium at a 1 : 100 dilution. After two to three successful transfers, the enrichments were serially diluted up to 10–11 using Hungate tubes with 10 ml medium. The latter was repeated several times until final purification of the dominant sulfidogenic bacteria was achieved, since none of them formed colonies in alkaline agar shake tubes. Culture purity was checked by microscopy and by sequencing of the 16S rRNA genes. The pH dependence of growth was examined at an Na+ content of 2 M, using the following filter-sterilized mineral media: for pH 6–8, 0.1 M HEPES and NaCl; for pH 8–11, a mixture of sodium bicarbonate/sodium carbonate containing 0.1 M NaCl. Growth resulted in a shift of the initial pH values, especially in the highly alkaline region. Therefore, final pH values were taken to indicate a suitable range for growth. To study the influence of salt concentration on growth, mineral media containing 0.1 and 4.0 M total Na+ at pH 10 were mixed in different proportions. The fate of acetate in pure cultures was investigated using cells from the late-exponential phase incubated with uniformly labelled [14C]acetic acid at 100 000 d.p.m. ml–1 final radioactivity. After 6 h of incubation, the supernatant was acidified and CO2 was captured in phenethylamine scintillator liquid. The distribution of 14C between assimilation into biomass and assimilation into inorganic carbon was then estimated.
Enzyme activity.
The activity of key enzymes of the reductive acetyl-CoA pathway, the reductive tricarboxylic acid cycle (TCA cycle), and hydrogenase in cell-free extract (CFE) of strain ASO3-1 was analysed spectrophotometrically at 30 °C, following the methods of Zeikus et al. (1977) and Schauder et al. (1987). CFE was obtained after sonication of the cell pellet in Tris buffer and subsequent centrifugation (16 000 g, 20 min, room temperature).
Analytical procedures.
Sulfide was precipitated in 10 % (w/v) Zn acetate, and subsequently analysed by the methylene blue method after separation from the supernatant (Trüper & Schlegel, 1964). Thiosulfate and sulfite were determined by iodimetry of the supernatant after separation of ZnS by centrifugation. First, the sum of sulfite and thiosulfate was measured, and then thiosulfate alone after the removal of sulfite with formaldehyde (3.7 %, v/v, final concentration). Cell protein was measured by the Lowry method after removal of interfering sulfur compounds. Several washing steps with 2 M NaCl acidified to pH 4 were necessary to remove FeS from the cell pellets. Membrane fatty acids were extracted from the freeze-dried cells with methanol/chloroform and analysed by GC-MS, as described by Zhilina et al. (1997). Organic-compatible solutes were extracted from the lyophilized cells by ethanol and analysed by HPLC (Galinski & Herzog, 1990). Phase-contrast photomicrographs were obtained with a Zeiss Axioplan Imaging 2 microscope. For electron microscopy of total cells, the cells were resuspended in 2 M NaCl, fixed with glutaraldehyde (3 %, v/v, final concentration) and positively contrasted with 1 % (w/v) uranyl acetate.
Genetic and phylogenetic analysis.
The isolation of the DNA and determination of the G+C content of the DNA were performed according to Marmur (1961) and Marmur & Doty (1962), respectively. For DNA–DNA hybridization, a thermal denaturation technique was employed (De Ley et al., 1970). For PCR, genomic DNA was extracted from the cells using the UltraClean Soil DNA Extraction kit (MolBio Laboratories), following the manufacturer's instructions. The nearly complete 16S rRNA gene was obtained from pure cultures using bacterial primers GM3F and GM4R. The PCR products were purified from low-melting agarose using the Wizard PCR-Prep kit (Promega). Sequencing was performed using the BigDye Terminator v3.1 Sequencing kit and an ABI 3730 automatic DNA sequencer (Applied Biosystems). The 16S rRNA sequences were first compared to sequences stored in the GenBank database using the BLAST search tool. The sequences were aligned with those from GenBank using CLUSTAL W. Phylogenetic trees were reconstructed with four different algorithms using the TREECONW software package (van de Peer & De Wachter, 1994). Pairwise evolutionary distances (expressed as estimated changes per 100 nucleotides) were computed by using the Jukes and Cantor method. The resulting phylogenetic tree was constructed by the neighbour-joining method. Bootstrap analysis (1000 replications) was used to validate the reproducibility of the branching patterns of the trees.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) and in Kulunda Steppe, Altai, Russia (lakes Tanatar-1, Picturesque, Bitter-1) (Foti et al., 2007, 2008). To get more information on the process, potential sulfidogenesis was measured in the sediment slurries obtained in July 2007 in lake Bitter-1 using sulfate and thiosulfate as electron acceptors and various electron donors. The results (Fig. 1) demonstrated the presence of a highly active sulfidogenic population at in situ salt–pH conditions. The rate of endogenous sulfate reduction (without external electron donors) was comparable with that obtained previously by the radiotracer technique. However, thiosulfate, but not sulfate, was the favoured electron acceptor. The potential rate of endogenous sulfidogenesis with thiosulfate was four times higher than with sulfate, while in the presence of external electron donors it became seven times higher. Another interesting conclusion from this experiment was that H2 and lactate, usually considered as the best electron donors for sulfate reduction, were much less efficient than formate and glucose (the latter probably indirectly through fermentation products), especially in the case of thiosulfate reduction.
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Cell morphology
All three pure cultures had vibrio-shaped cells of variable size with a single polar flagellum. Cells of ASO3-1 and AHT 8 were considerably larger than those of AHT 6, and became long spirilla in the presence of an organic electron donor (Fig. 2).
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). Sequence similarity was 99.4 % between AHT 8 and ASO3-1, and 98.5 % between AHT 6 and ASO3-1.
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Compatible solutes
Analysis of intracellular compatible solutes in strains ASO3-1 grown with lactate and sulfite at 3 M total Na+ indicated the presence of glycine betaine at a high specific concentration (16 % from the total cell mass). This is a first indication of the presence of this osmolyte in the Deltaproteobacteria.
Growth characteristics and metabolic properties
The most interesting property of the isolates was their ability to grow by dismutation of sulfite and thiosulfate (inorganic fermentation) on purely mineral medium. The strains tolerated 12–15 mM sulfite and formed 0.20–0.22 mol sulfide per mol sulfite consumed, which closely corresponded to the theoretical value of 25 % derived from the stoichiometry of the reaction (4
HS–+3
). Dismutation of thiosulfate yielded approximately 0.92 mol sulfide per mol thiosulfate consumed, also in good agreement with the theoretical stoichiometry (
HS–+
). All isolates were able to grow as true SRB, using several electron donors, including hydrogen, formate, lactate and ethanol (Table 1). The addition of external electron donors abolished disproportionation of sulfite or thiosulfate and sulfur, and only sulfide was formed. The strains tolerated high concentrations of sulfite. The switch of the cultures from sulfite or thiosulfate to sulfate was very slow. The growth dynamics of strain ASO3-1 under different conditions are shown in Fig. 4. Its specific growth rates at 2 M Na+ and pH 10 with sulfite or thiosulfate alone were 0.010 and 0.006 h–1 (doubling times of 67 and 112 h), respectively. The addition of lactate increased the growth rate 1.5- to twofold. The specific biomass yield during disproportionation was 1.3 mg protein (per mmol 
) and 0.8 mg protein (per mmol 
). The influence of acetate on the growth of the isolates was of special interest, since AHT 6 was isolated as a presumed ‘acetate-utilizing’ SRB. However, with this strain we obtained the same result as during the first discovery of thiosulfate-disproportionating SRB by Bak & Pfennig (1987): the bacterium was able to grow without acetate, which was utilized as a carbon source only during chemolithoheterotrophic growth. This was also the case for the other strains, isolated without acetate. For example, in AHT 6, the biomass yield per mol thiosulfate increased 1.5- to twofold when 1–5 mM acetate was added, while no further increase up to 20 mM acetate was obtained. With strain ASO3-1 grown with sulfite, the effect of acetate addition was much less evident: only a 30 % increase in biomass yield and rate of sulfite consumption was obtained. The experiments with [14C]acetate confirmed that acetate served as a carbon source only in the case of AHT 6.
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) demonstrated that the cells grown with thiosulfate as electron acceptor actively reduced thiosulfate, sulfite and much less actively sulfate, while the cells grown with sulfite could only reduce sulfite and sulfate. This indicated that thiosulfate reductase activity was inducible, and that the reduction of thiosulfate most probably goes through sulfite. The cells grown on thiosulfate exhibited extremely high sulfidogenic activity with elemental sulfur. However, growth with sulfur as acceptor was not observed. Clearly, the enzymic system involved in thiosulfate disproportionation is able to actively reduce elemental sulfur. This property is known, for example, for the dissimilatory thiosulfate-reducing complex Phs (Hinsley & Berks, 2002). On the other hand, the toxicity of produced polysulfide (a spontaneous reaction product of sulfide and sulfur) might be a reason for the failure of growth with sulfur as acceptor in all species of alkaliphilic SRB so far described.
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Influence of pH and salt on growth and sulfidogenic activity
The pH profile for growth and sulfidogenic activity measured for strains ASO3-1 and AHT 6 at 2 M total Na+ was typical for obligate alkaliphiles, with a pH range from 8.0–8.5 to 10.5 and an optimum at pH 9.5–10 (Fig. 5b). The sodium concentration range for growth and sulfidogenic activity tested in sodium carbonate-based medium at pH 10 was different for the two strains. While strain ASO3-1 can be qualified as an extreme natronophile unable to grow properly at salt contents below 1.5 M Na+ and growing at up to 4 M Na+, AHT 6 was less salt-dependent, starting to grow actively at 0.8 M and tolerating up to 3.5 M total Na+ (Fig. 5a). Such a high salt tolerance as that observed in these isolates has not, as far as we know, been reported before for the known alkaliphilic SRB.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The question of where sulfite and thiosulfate come from is not new. It has been treated before for marine sediments (Jørgensen, 1990). However, in soda lakes, thiosulfate could be a particularly important intermediate, since it is the main product of spontaneous polysulfide oxidation. Polysulfide (
) is a sulfur species that is stable under anoxic alkaline conditions; it is formed by the spontaneous reaction of elemental sulfur with sulfide. Once sulfide is formed by reduction of sulfate, the active cycling of thiosulfate might commence after partial oxidation of sulfide to sulfur in the micro-oxic zone. Active polysulfide/thiosulfate formation was recently documented in a laboratory-scale sulfide-oxidizing bioreactor operating under extremely natronophilic conditions (Van den Bosch et al., 2007).
In our previous work on the molecular diversity of SRB in soda lake sediments using the dsrAB gene as a molecular marker (Foti et al., 2007), a large group of organisms clustered with the low salt-tolerant Desulfonatronovibrio hydrogenovorans isolated from the hypersaline soda lake Magadi. However, from these data it was not possible to predict whether those bacteria are different with respect to salt tolerance. Analysis of the dsrAB gene of a pure culture of the extremely natronophilic strain ASO3-1 demonstrated that it is indeed a member of the cluster within the family Desulfohalobiaceae found in the soda lake sediments (Foti et al., 2007). This family accommodates two groups of neutrophilic SRB able to cope with the highest NaCl concentrations among the known SRB, the genera Desulfohalobium (Ollivier et al., 1991) and Desulfovermiculus (Belyakova et al., 2006). The extremely natronophilic isolates from the hypersaline soda lakes form a new phylogenetic lineage within this extremophilic SRB family.
The ability to grow by disproportionation of sulfur compounds has been described before for only a few SRB species (Bak & Pfennig, 1987; Janssen et al., 1996; Finster et al., 1998), including the low salt-tolerant moderate alkaliphile Desulfonatronum thiodismutans (Pikuta et al., 2003) and some other species that can disproportionate sulfur compounds without growth, such as Desulfonatronovibrio hydrogenovorans (Sydow et al., 2002). So far, the only known species able to grow by dismutation of sulfite and thiosulfate chemoautotrophically is the obligately disproportionating Desulfocapsa sulfoexigens. Our growth experiments (the potential to grow in the absence of organic carbon source) and enzymic tests (i.e. the presence of the Wood cycle enzymes) indicated that the extremely natronophilic isolates from the hypersaline soda lakes are capable of an autotrophic mode of growth. However, this must be substantiated by evidence of inorganic carbon incorporation into the cells. The stoichiometry of sulfide production during sulfite and thiosulfate dismutation was slightly lower than the theoretical values, which could be explained by the consumption of reducing equivalents needed for inorganic carbon reduction for cell mass synthesis. Despite the fact that the novel isolates grew under doubly extreme conditions (pH, salt), the specific growth yield during dismutative growth was close to the values obtained for non-extremophilic SRB species (Bak & Pfennig, 1987), indicating an efficient energy conservation mechanism. The latter is indeed needed for these bacteria, since the formation of high amounts of the organic osmolyte glycine betaine requires substantial energy (Oren, 1999). Two facts might be taken into consideration in this respect: (i) the virtual lack of toxic H2S species at pH 10 (which is important for the dismutating SRB); and (ii) the more negative 
G values that result from the low proton concentration (which is important if the catabolic reaction takes place in the periplasm facing external alkaline conditions). On the other hand, extreme conditions can definitely be held responsible for the very low specific growth rates observed, which were five to 10 times lower than in the non-extremophilic SRB species growing by dismutation.
In conclusion, extremely natronophilic SRB found in hypersaline soda lakes are proposed to form a novel genus within the family Desulfohalobiaceae, class Deltaproteobacteria, for which the name Desolfonatronospira is suggested. The closely related strains ASO3-1 and AHT 8 form a novel species Desulfonatronospira thiodismutans, while strain AHT 6 is proposed as another species Desulfonatronospira delicata.
Description of Desulfonatronospira gen. nov.
Desulfonatronospira (de.sul.fo.na.tro.no.spi'ra L. prep. de, from; N.L. pref. sulfo-, prefix used for N.L. masc. n. sulfas – atis, sulfate; N.Gr. n. natron, arbitrarily derived from the Arabic n. natrun or natron, soda; L. fem. n. spira, a spire; N.L. fem. n. Desulfonatronospira, desulfurizing soda-loving spirillum).
Gram-negative bacterium with vibrio-shaped cells of variable size. Obligately anaerobic with respiratory or fermentative metabolism. Uses sulfur oxyanions as electron acceptor, and short-chain fatty acids and H2 as electron donors. Can grow by dismutation of sulfite and thiosulfate. Obligately alkaliphilic and extremely salt-tolerant. Belongs to the family Desulfohalobiaceae, order Desulfovibrionales within the Deltaproteobacteriae. The type species is Desulfonatronospira dismutans. Habitat: hypersaline soda lakes.
Description of Desulfonatronospira thiodismutans sp. nov.
Desulfonatronospira thiodismutans (thi.o.dis.mu'tans Gr. n. thios, sulfur; L. particle dis, in two, apart; L. part. adj. mutans, changing, altering; N.L. part. adj. thiodismutans, dismutating sulfur).
Cells are Gram-negative, vibrio-shaped, with size variable from single vibrio to long spirillum, depending on growth conditions, 0.6–0.8x2–30 µm, motile by a single polar flagellum. Strictly anaerobic with respiratory or fermentative metabolism. Respiration with sulfate/sulfite/thiosulfate as acceptors is possible during autotrophic growth with either formate or hydrogen as electron donor, or with simple organic compounds such as lactate, ethanol and butanol. Acetate alone can be used as a carbon source. Fermentative growth occurs either by the inorganic chemolithoautotrophic mode through dismutation of sulfite or thiosulfate to sulfide and sulfate or by the organic mode through fermentation of pyruvate. Obligately alkaliphilic, with a pH range for growth between 8.3 and 10.5 and an optimum at pH 10, and extremely natrono (soda)philic with a total Na+ range for growth from 1.5 to 4.0 M (optimum at 2.0–2.5 M). Mesophilic, with a maximum temperature for growth of 43 °C. The dominant fatty acids in the membrane lipids include isoC15 : 0, isoC17 : 1 and C16 : 0. Cells accumulate high concentrations of glycine betaine as a compatible solute. The G+C content of the genomic DNA is 49.8–50.4 mol% (Tm). The species includes two closely related strains. The type strain ASO3-1T (DSM19093T=UNIQEM U234T) and strain AHT 8 were isolated from the Kulunda Steppe soda lakes (Altai, Russia). The GenBank 16S rRNA sequence accession numbers of these strains are EU296537 and EU296538, respectively.
Description of Desulfonatronospira delicata sp. nov.
Desulfonatronospira delicata (del.i.ca'ta. L. fem. adj. delicata, delicate).
Cells are Gram-negative, vibrio-shaped, 0.4–0.6x1.2–4.0 µm, motile by a single polar flagellum. Strictly anaerobic with respiratory metabolism or fermentative metabolism. Respiration with sulfate/sulfite/thiosulfate as acceptors is possible during autotrophic growth with either formate or hydrogen as electron donor, or with simple organic compounds such as lactate, pyruvate and ethanol. Acetate can be used as a carbon source. Fermentative growth occurs either by the inorganic chemolithoautotrophic mode through dismutation of sulfite/thiosulfate to sulfide and sulfate or by the organic mode through fermentation of pyruvate. Obligately alkaliphilic, with a pH range for growth between 8.0 and 10.6 and an optimum at pH 10, and extremely natronotolerant with a total Na+ range for growth from 0.8 to 3.5 M (optimum at 1.0 M). Mesophilic, with a maximum temperature for growth of 45 °C. The dominant fatty acids in the membrane lipids include isoC15 : 0, 10MeC16 : 01 and isoC17 : 0. The G+C content of the genomic DNA is 50.2 mol% (Tm). The type strain AHT 6T (DSM19491T=UNIQEM U275T) was isolated from the Wadi al Natrun haloalkaline lakes in Egypt. The GenBank 16S rDNA sequence accession is EU296539.
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ACKNOWLEDGEMENTS |
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Edited by: H.-P. Klenk
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Received 5 December 2007;
revised 29 January 2008;
accepted 23 February 2008.
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), thiosulfate alone (
), lactate+sulfite (
) and H2+thiosulfate (
).