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1 Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospect 60-let Octyabrya 7/2, 117811 Moscow, Russia
2 Department of Environmental Biotechnology, Delft University of Technology, Julianalaan 67, 2628 BC Delft, The Netherlands
3 MPI für Terrestrische Mikrobiologie, Karl-von-Frisch-Straße, D-35043 Marburg, Germany
Correspondence
Dimitry Yu. Sorokin
soroc{at}inmi.host.ru
or
D.Y.Sorokin{at}tnw.tudelft.nl
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences obtained in this study are DQ469580–DQ469581, DQ836238, EF117909–EF117913 and EF455919, and for the nirS gene from strain HLD 2T, AM492191.
Cytochrome difference spectra of cell-free extract obtained from strain HLD 2T cells grown anaerobically with nitrate and thiosulfate, and graphs showing the influence of NaCl on anaerobic growth of HLD strains with nitrate and thiosulfate, and on the activity of thiosulfate oxidation by washed cells of strain HLD 2T grown anaerobically are available with the online version of this paper.
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). Some of the moderately halophilic/extremely salt-tolerant Gammaproteobacteria, such as Halomonas and Marinobacter, better adapted to lower salinity, have an advantage over less flexible haloarchaea at fluctuating salinity (Ventosa et al., 1998). Recent studies have demonstrated that moderately and extremely halophilic bacteria represent an important component of prokaryotic communities, even under extremely high-salt conditions (Antón et al., 2002; Sorokin et al., 2006a). Furthermore, even chemolithoautotrophic bacteria can be abundant and active under such conditions. In particular, chemolithoautotrophic sulfur-oxidizing bacteria (SOB) have the best chance to adapt to extremely high-salt conditions because of a very high energy yield available during complete oxidation of sulfide/thiosulfate to sulfate (Oren, 1999).
Previously, we demonstrated the potential of haloalkaliphilic SOB belonging to the genus Thioalkalivibrio for growth in saturated soda brines (Sorokin & Kuenen, 2005). In addition, a large diversity of moderately and even extremely halophilic SOB has been discovered in hypersaline habitats with neutral pH (Sorokin et al., 2006b). Among the six different types of halophilic SOB discovered, two groups of aerobic moderate halophiles belong to the known genera Thiomicrospira (Sorokin et al., 2006c) and Halothiobacillus. The latter contains the only SOB species, Halothiobacillus halophilus, which was known previously as being capable of growing at NaCl concentrations up to 4 M (Wood & Kelly, 1991). The other four novel groups belong to previously unknown lineages within the Gammaproteobacteria. They include two groups of moderately halophilic thiodenitrifiers and two groups of extreme halophiles.
Here we describe the properties of a novel group of moderately halophilic, obligately chemolithoautotrophic and facultatively anaerobic, sulfur-oxidizing Gammaproteobacteria, consisting of 11 isolates from sediments of hypersaline lakes and a solar saltern. These bacteria dominated the anaerobic enrichment cultures with thiosulfate as electron donor and nitrate as electron acceptor at 2 M NaCl.
Sediments from hypersaline lakes in north-east Mongolia, the Kulunda Steppe (south-west Siberia, Altai, Russia) and the Crimea (Ukraine), Lake Baskunchak (South Russia) and the Se
ovlje Adriatic Sea solar saltern were used as inoculum in this work (Sorokin et al., 2006b). In general, the salt content of the brines varied from 10 to 38 % (w/v) and the pH ranged from 6.5 to 8.2; the dominant ions were Na+, Mg2+, Cl– and 
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The following mineral base medium was used for enrichment and growth experiments: NaCl, 0.5–3.0 M; K2HPO4, 10 mM; NH4Cl, 5 mM. The pH was adjusted to 7.2–7.5 with 10 % KH2PO4. After sterilization, the medium was supplemented with 2 mM MgCl2.6H2O and 1 ml trace metal solution l–1 (Pfennig & Lippert, 1966). Thiosulfate (5–20 mM) or thiocyanate (5–10 mM) were added as electron donors (the range is for aerobic and anaerobic conditions, respectively), and KNO3 (20 mM), KNO2 (5 mM), N2O (10 % in the gas phase) or O2 (2–20 % in the gas phase) were used as electron acceptors. Filter-sterilized NaHCO3 (10–40 mM, pH 8.0; the range depending on the amount of thiosulfate added) was used as the carbon source and as the pH buffer. Anaerobic cultivation was routinely performed in 100 ml serum bottles with 80 ml medium, which was made anoxic by five sequential cycles of evacuation–flushing with argon. In the case of aerobic incubations, the liquid/gas ratio was 10 : 90. Cultivation was performed at 30 °C. Growth was monitored by following the optical density at 600 nm and by qualitative tests for nitrate/nitrite (Merck). Positive enrichment cultures were stabilized by several 1 : 100 transfers and, finally, pure cultures were obtained after several dilution to extinction series. The purity of the cultures was checked by the absence of growth on medium where thiosulfate was replaced by yeast extract (1 g l–1) and further confirmed by sequencing. Dialysis cultivation and use of sucrose gradient centrifugation to separate a nitrate-reducing strain from the mixed denitrifying enrichment were performed as described previously (Sorokin et al., 2006b).
Nitrogen (nitrate, nitrite, N2O) and sulfur (sulfide, sulfur, thiosulfate, sulfate, thiocyanate, tetrathionate) compounds in growth experiments were analysed as described previously (Sorokin et al., 2001a, b, 2004). Protein concentrations were measured by the Lowry method after removal of interfering sulfur compounds either by washing (thiosulfate, thiocyanate) or by overnight extraction with acetone (sulfur). Cellular fatty acids were extracted with a mixture of methanol/chloroform and analysed by GC-MS according to Zhilina et al. (1997). Phase-contrast micrographs were obtained using an Axioplan Imaging 2 microscope (Zeiss). For electron microscopy, the cells were subjected to cryofixation in glutaraldehyde (final concn 3 %, v/v) at pH 7.0 in the presence of 0.5 M NaCl, then post-fixed in 1 % (w/v) OsO4/0.5 M NaCl for 3 h at room temperature, washed and stained overnight with 1 % (w/v) uranyl acetate, dehydrated in an ethanol series and embedded in Epon resin. Thin sections were contrasted with 1 % (w/v) lead citrate.
The isolation of genomic DNA and subsequent determination of the G+C content of the DNA were carried out according to Marmur (1961). DNA–DNA hybridization was performed by the thermal denaturation/reassociation technique (De Ley et al., 1970). Genomic DNA for PCR amplification 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 (Schäfer & Muyzer, 2001). PCR products were purified from low-melting-point agarose using the Wizard PCR-Prep kit (Promega) according to the manufacturer's instructions. Sequencing was performed using the BigDye Terminator v.3.1 Cycle Sequencing Kit with an ABI 3730 DNA automatic sequencer (Applied Biosystems). 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 nt) were computed by using the method of Jukes & Cantor (1969). The resulting phylogenetic tree was constructed by the neighbour-joining method. Bootstrap analysis (100 replications) was used to validate the reproducibility of the branching patterns of the trees.
Cytochrome cd1-containing nitrite reductase genes (nirS) were amplified from 50 ng genomic DNA from strain HLD 2T using primer pair nirS1F and nirS6R and protocols described previously by Braker et al. (1998). PCR products of the expected size (approx. 890 bp) were purified with the QIAquick PCR purification kit (Qiagen). Both strands were sequenced directly from the PCR product on an ABI 3100 automated DNA sequencer (Applied Biosystems) using gene-specific primers nirS1F and nirS6R and the BigDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems). Forward and reverse strand sequences were assembled by using Seqman II software (DNASTAR) and aligned to sequences from the embl database with the ARB fast aligner feature (www.arb-home.de). For phylogenetic analysis a filter was calculated to omit insertions or deletions (indels) due to ambiguous positional homology and included 241 aa positions. Analyses were performed with the PHYLIP software package version 3.66 (Felsenstein, 1989). Trees were reconstructed by using the distance-matrix-based neighbour-joining method with the Jones–Taylor–Thornton amino acid replacement model, the parsimony method PROTPARS and the maximum-likelihood method PROTML. Statistical evaluation of tree topologies was performed with 1000 resamplings for each method.
Only nitrate supported thiosulfate oxidation in anaerobic enrichments at 2 M NaCl with thiosulfate as electron donor and NOx as electron acceptors. Positive enrichments were obtained from various lake sediments and from the solar saltern. In all cases nitrite and N2O were observed as major intermediates of nitrate reduction with N2 as the final product. Thiosulfate was oxidized to sulfate with occasional formation of elemental sulfur (at high levels of nitrite production) as an intermediate. Despite vigorous growth in liquid culture, colony formation could not be achieved, neither on the agar plates in anaerobic jars nor in agar shake tubes. The isolation of pure cultures was only possible after several rounds of serial dilution to extinction with a reduced concentration of nitrate (i.e. 5 instead of 20 mM) to avoid inhibition by nitrite. Finally, 10 strains (abbreviated as HLD) were isolated in pure culture (Table 1).
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). Under unfavourable growth conditions, such as the substitution of Cl– by 
or Na+ by K+ (above 50 %), the formation of cyst-like round cells (Fig. 1b) covered with an extracellular matrix layer (Fig. 1e) was observed. Thin sectioning of one of the strains revealed two interesting ultrastructural features inside the cells. The cytoplasm in the cell tips had a distinct grainy texture, which was clearly different from the more homogeneous middle zone containing the genomic DNA (Fig. 1d). It might be that the growing tips of the cells contain a high number of ribosomes in contrast to the ‘old’ middle part. Furthermore, in many cells a single- or double-ring structure could be seen (Fig. 1f), which might be mesosomes – a cell membrane extension binding to the chromosome (Silva et al., 1976).
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). Phylogenetic analysis of seven isolates from different geographical locations revealed that they formed a separate lineage within the Gammaproteobacteria with ‘Thiobacillus prosperus’ as the closest culturable relative (92 % sequence homology) (Fig. 2a). Analysis of the fatty acid composition of the polar lipids in strain HLD 2T demonstrated a pattern typical for the moderately halophilic Gammaproteobacteria (such as Halomonas), with C16 : 0, C16 : 1 and C18 : 1 dominant (Table 2).
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).
The HLD strains grew best anaerobically with thiosulfate and nitrate. Growth was not observed with either H2 or organic compounds (i.e. acetate, pyruvate and yeast extract) used as electron donors instead of thiosulfate. Sulfate was the final product of thiosulfate oxidation. However, accumulation of nitrite at a high initial nitrate concentration (i.e. 10–20 mM) was a common problem for all the strains. Nitrite started to inhibit growth at concentrations above 4–5 mM and caused incomplete oxidation of thiosulfate to sulfur and growth inhibition. This can be avoided by providing the nitrate in small portions at low concentrations (3–5 mM) after complete reduction of the produced nitrite to N2. In this way the HLD cultures had a relatively high growth yield [4–5 mg protein (mmol 
)–1] and a maximum growth rate of 0.03–0.04 h–1 at 2 M NaCl. Despite the fact that nitrite and N2O were produced as intermediates during anaerobic growth with nitrate, and that washed cells, grown with nitrate, could reduce both intermediates in the presence of thiosulfate, anaerobic growth could be initiated only with nitrate. Growth with oxygen instead of nitrate as electron acceptor was less regular. In the case of a few successful incubations, growth was observed under micro-oxic conditions at O2 concentrations between 2 and 5 % (v/v) in the gas phase. The HLD strains grew within a relatively narrow salt range from 1.0 to 3.0 M NaCl, with an optimal concentration of 1.5–2 M (supplementary Fig. S2a, available with the online version of this paper). Some of them still oxidized thiosulfate at lower salinity with the production of nitrite and elemental sulfur, but without substantial biomass growth. Washed cells, grown anaerobically with nitrate at 2 M NaCl, oxidized thiosulfate most actively with N2O as electron acceptor. With all four different electron acceptors (O2, 
, 
and N2O) washed cells exhibited maximum activity at very high salt concentrations, but were lysed rapidly at 0.5 M NaCl (supplementary Fig. S2b, available with the online version of this paper). The pH values suitable for growth tested under aerobic conditions for strains HLD 2T and HLD 16 were limited to a range from 6.5 to 8.2, with an optimum between 7.3 and 7.8.
When thiosulfate was replaced by thiocyanate (NCS–), only a single anaerobic enrichment (from a mixture of sediment samples from the Kulunda Steppe lakes) gave a positive result at 1–2 M NaCl, in which the oxidation of thiocyanate to sulfate was linked to a complete reduction of nitrate to N2 gas. Serial dilutions were positive only up to 10–4 with four to five different morphotypes still present. However, replacement of thiocyanate by thiosulfate allowed selection of a binary co-culture, which reduced nitrate to N2 without intermediate nitrite accumulation at 1–2 M NaCl. In this case the co-culture was more efficient than single HLD strains. The association consisted of thin rods as the dominant morphotype, and thick vibrios as a minor component. The co-culture was very stable and very difficult to separate into individual species. Final resolution of the co-culture resulted in the isolation of a pure culture of the nitrate-reducing, vibrio-shaped strain HRhD 3spT (by sucrose gradient centrifugation) and the rod-shaped, nitrite-reducing strain HRhD 2. The latter has recently been described as a new genus and species ‘Thiohalophilus thiocyanoxidans’ (Sorokin et al., 2007). Strain HRhD 3spT had vibrio-shaped, non-motile cells, the length of which depended on the growth conditions (Fig. 3). It had a capacity for anaerobic growth with thiosulfate (but not with thiocyanate) and nitrate, which was limited by high sensitivity to accumulating nitrite and an inability to reduce it further. Accumulation of 2.5–3.0 mM nitrite completely arrested growth and resulted in an incomplete oxidation of thiosulfate to elemental sulfur. This was probably the main reason for this bacterium growing in association with the nitrite-consuming thiodenitrifier. This conclusion was confirmed by growing HRhD 3spT in a dialysis culture in which nitrite diffused out of the culture vessel; the culture reached a five times higher cell density than in ordinary batch mode. Growth in the presence of oxygen was irregular and only possible at oxygen concentrations below 5 % in the gas phase. The NaCl tolerance range and optimum concentration of the nitrate-reducing isolate were lower than for the HLD strains (1.0–2.5 and 1.0 M, respectively). Phylogenetic analysis demonstrated that strain HRhD 3spT is a member of the HLD cluster with a separate species status (97 % 16S rRNA gene sequence homology; see Fig. 2a), which was also confirmed by DNA–DNA hybridization with HLD 2T (40 % homology).
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Description of Thiohalomonas gen. nov.
Thiohalomonas [Thi.o.ha.lo.mo'nas. Gr. n. thion sulfur; Gr. n. hals, halos salt; Gr. n. monas a unit, monad; N.L. fem. n. Thiohalomonas salt (-tolerant), sulfur-utilizing monad].
Cells are non-motile rods or vibrios with a Gram-negative cell wall. Obligately chemolithoautotrophic and facultatively anaerobic. Utilizes reduced sulfur compounds as electron donors with oxygen or nitrate as electron acceptors. Moderately halophilic and neutrophilic. Member of the Gammaproteobacteria. Habitat is hypersaline lakes and salterns. Type species is Thiohalomonas denitrificans.
Description of Thiohalomonas denitrificans sp. nov.
Thiohalomonas denitrificans (de.ni.tri'fi.cans N.L. v. denitrifico to denitrify; N.L. part. adj. denitrificans denitrifying).
In addition to the genus description, cells are long, non-motile rods of variable size (0.4–0.5x2–6 µm) with a Gram-negative type of cell wall. Obligately chemolithoautotrophic. Utilizes sulfide and thiosulfate as electron donor with sulfate as the final oxidation product. Grows best anaerobically with nitrate as electron acceptor. Reduces nitrate completely to N2 with intermediate production of nitrite and N2O. Can grow with oxygen as electron acceptor under micro-oxic conditions. Moderately halophilic with a salinity range for growth from 1.0 to 3.0 M NaCl, and an optimum at 1.5–2.0 M. The pH range for growth is between 6.5 and 8.2 with an optimum between 7.3 and 8.2. The dominant cellular fatty acids are 16 : 0, 16 : 1
7 and 18 : 17. The G+C content of the DNA is 58–60 mol% (Tm). Includes ten strains isolated from the sediments of hypersaline lakes and a solar saltern in Eurasia.
The type strain is HLD 2T (=DSM 15841T=UNIQEM U222T). Isolated from sediments of hypersaline lakes in south-west Siberia. 16S rRNA gene sequence accession number is EF117909.
Description of Thiohalomonas nitratireducens sp. nov.
Thiohalomonas nitratireducens (ni.trat.i.re.du'cens. N.L. n. nitras nitrate; L. part. adj. reducens converting to a different state; N.L. part. adj. nitratireducens reducing nitrate).
In addition to the genus description, cells are non-motile vibrios of variable length (0.5x1–5 µm) with a Gram-negative type of cell wall. Obligately chemolithoautotrophic. Utilizes thiosulfate as electron donor with sulfate as the final oxidation product. Grows anaerobically with nitrate as electron acceptor, reducing it incompletely to nitrite. Anaerobic growth is inhibited by nitrite at concentrations above 2.5 mM. Can grow with oxygen as electron acceptor under micro-oxic conditions. Moderately halophilic with a salinity range for growth from 1.0 to 2.5 M NaCl and an optimum at 1.0 M. The pH optimum for anaerobic growth is 7.8–8.0. The G+C content of the DNA is 62.9 mol% (Tm).
The type strain is HRhD 3spT (=DSM 16925T=UNIQEM U248T). Isolated from sediments of hypersaline lakes in south-west Siberia. 16S rRNA gene sequence accession number is DQ836238.
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ACKNOWLEDGEMENTS |
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Sorokin, D. Yu., Tourova, T. P., Galinski, E. A., Belloch, C. & Tindall, B. J. (2006a). Extremely halophilic denitrifying bacteria from hypersaline inland lakes Halovibrio denitrificans sp. nov. and Halospina denitrificans gen. nov., sp. nov., and evidence that the genus name Halovibrio (Fendrich 1989) with the type species H. variabilis should be associated with DSM 3050. Int J Syst Evol Microbiol 56, 379–388.
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). N, Nucleoid; R, ribosome-like structures; C, capsule; M, mesosome-like structures; arrows indicate separation of the cells into two different parts.
