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1 Astrobiology Laboratory, NASA/NSSTC, 320 Sparkman Drive, Huntsville, AL 35805, USA
2 Department of Biology, University of Alabama at Birmingham, Birmingham, AL 35294, USA
3 Department of Biological Sciences and Laboratory for Structural Biology, University of Alabama in Huntsville, MSB, Huntsville, AL 35899, USA
4 Department of Microbiology, University of Georgia, Athens, GA 30602-2605, USA
5 American Type Culture Collection, 10801 University Boulevard, Manassas, VA 20110, USA
Correspondence
Elena V. Pikuta
elena.pikuta{at}msfc.nasa.gov
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain MLF1T is AF373920.
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; Castro et al., 2000; Pikuta & Hoover, 2001). Among this group, there are two genera that contain obligately alkaliphilic species. The first alkaliphilic sulfate-reducer, Desulfonatronovibrio hydrogenovorans, was isolated from soda Lake Magadi in equatorial Africa (Zhilina et al., 1997). Later, the distribution of this species was extended to Tuva's soda lakes in Siberia, central Asia (Pikuta et al., 1997) and a novel alkaliphilic species, Desulfonatronum lacustre, was described (Pikuta et al., 1998). Both genera include Gram-negative, non-spore-forming, mesophilic, obligately carbonate-dependent alkaliphiles that are incapable of growth below pH 8·0. The moderately thermophilic and alkaliphilic, spore-forming sulfate-reducer Desulfotomaculum alkaliphilum was isolated from manure with neutral pH (Pikuta et al., 2000), indicating that the adaptation of micro-organisms to alkalic environments is not connected with deep genetic changes and that local micro-ecosystems with high pH and temperature could be created in composite substrates, such as soil or manure, by these micro-organisms. All previously described alkaliphilic sulfate-reducers had a lithoheterotrophic metabolism. In this article we describe a novel alkaliphilic, mesophilic, sulfate-reducing bacterium with the capacity for lithoautotrophic growth.
Isolation, cultivation and morphology
Black mud sediments (pH 9·9±0·02) with a strong smell of sulfide were collected anaerobically from under shallow water (temperature, 21·6±0·1 °C; salinity, 7 %) near the south shore of Mono Lake in California on 15 August 2000. Mud samples were hermetically sealed in sterile glass vessels with screw caps, maintained at 4 °C during transportation and stored at 2 °C in the Astrobiology Laboratory of the NASA Marshall Space Flight Center. For cultivation of the novel isolate, modified medium was used (Pikuta et al., 1998), which contained (l-1): Na2SO4, 3 g; NaCl, 30 g; Na2CO3, 2·76 g; NaHCO3, 24·0 g; KCl, 0·2 g; K2HPO4, 0·2 g; MgCl2.6H2O, 0·1 g; NH4Cl, 1·0 g; Na2S.9H2O, 0·4 g; resazurin, 0·001 g; yeast extract, 0·2 g; Na-formate, 5·0 g; 2 ml vitamin solution (Wolin et al., 1963); and 1 ml trace mineral solution (Whitman et al., 1982). The final pH was adjusted to 9·5. High-purity nitrogen was used as the gas phase, except in the case of cultivation with hydrogen as the electron donor, for which the gas phase was filled by pure hydrogen. To obtain enrichment cultures, 0·5 g wet sediment material (pH 10·0) was injected into standard Hungate tubes that contained medium and incubated at 35 °C for 10–14 days. Pure cultures were obtained by the dilutions method on sulfate-containing medium with hydrogen as the electron donor. Growth of colonies was checked by the ‘roll-tube’ method on 3 % (w/v) agar medium, where carbonates were added separately after autoclaving. Colonies were white-yellowish, lens-shaped in deep agar and 0·5–2·0 mm in diameter with irregular, smooth edges. One colony was chosen for further characterization and designated strain MLF1T (=ATCC BAA-395T=DSM 14708T). Purity of the culture during this study was indicated by the absence of growth on glucose–peptone sulfate-free medium that contained excessive quantities of yeast extract and by microscopic control.
Transmission electron microscopy was carried out by using a JEOL TEM 100 CX II. Negative staining was performed with uranyl acetate. Cells of strain MLF1T were highly motile and vibrio-shaped, 0·6–0·7 µm in diameter and 1·2–2·7 µm long and had a single polar flagellum (Fig. 1). Cells occurred singly, in pairs or as short spirilla. Multiplication occurred by binary fission. Gram-stained cells of strain MLF1T exhibited the red colour typical for the reaction with Gram-negative cell walls. Spores were not observed.
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) or by estimating an increase in OD510 (Genesis 5; Spectronic Instruments). All experiments were performed at 35 °C. Obligate dependence on the 
ion was detected by using a medium that was described previously (Pikuta et al., 2000). Dependence on Na+ ions was detected by substitution of Na-containing salts by K-containing salts. Dependence on Cl- ions was checked by substitution of Cl-containing salts by sulfates. The novel isolate grew only under strictly anaerobic conditions and was catalase-negative (Gerhardt et al., 1981). The isolate was mesophilic and grew at 15–45 °C, with optimum growth at 37 °C; growth was absent at 10 and 53 °C. The novel isolate grew at pH 8·0–10·0; no growth was detected at pH values of 7·8 or 10·5. Strain MLF1T required Na+ ions (from NaCl) for growth; it did not grow at 0 % (w/v) NaCl. The optimum NaCl concentration was 3 % (w/v), the range for growth was 1–7 % (w/v) and growth was absent at 10 % (w/v) NaCl. The generation time at optimal conditions [37 °C, 3 % (w/v) NaCl and pH 9·5] was 20 h. The novel isolate was obligately dependent on Na+ ions, as it did not grow on medium with potassium salts instead of sodium salts. The absence of growth on serine-buffered medium demonstrated obligate dependence on 
ions. Strain MLF1T was not dependent on Cl- ions, but cell motility was significantly decreased on medium without Cl-containing salts. The novel isolate required sulfates for respiration. End-products of sulfate respiration in the liquid phase were determined by HPLC. Sodium salts (formate, acetate, lactate, pyruvate, propionate and isovalerate) were used as standards. Separation was done on an Aminex HPX-87H column (Bio-Rad), with 5 mM H2SO4 as the mobile phase. Gases (hydrogen, carbon dioxide, carbon monoxide and methane) were measured by using a model 3700 gas chromatograph (Varian) equipped with a Porapak Q column and a thermal conductivity detector. Nitrogen was used as the gas carrier. During sulfate respiration with formate, strain MLF1T excreted only hydrogen sulfide (more than 30 mM) and no organic end-products were detected. CO2 measurement at high pH was not feasible because of the high carbonate content of the medium.
Strain MLF1T had a lithoautotrophic type of metabolism. Growth was observed during three consequent inoculations on hydrogen medium with no organic carbon source. Growth on media without an organic carbon source was slow (10–14 days) with lower optical density (0·08–0·1) and the number of cells was approximately 108 ml-1. During lithoautotrophic growth (H2+CO2), high sulfidogenesis (10–15 mM H2S) was registered. Strain MLF1T also grew on H2 media with yeast extract or acetate (2 mM). Organic carbon sources stimulated growth, with more rapid growth occurring on media with yeast extract than with acetate (optical density of growth on acetate was 0·2–0·25, and on yeast extract it was 0·3–0·5). Strain MLF1T does not have a fermentative type of metabolism for organic substrates and has a very restricted spectrum of electron donors: only hydrogen, formate and ethanol were utilized. Growth did not occur on acetate, propionate, butyrate, pyruvate, lactate, methanol, glycerol, glycine, cysteine, cystine, serine, alanine, glutamate, aspartate, Casamino acids, yeast extract, peptone, bacto-tryptone, betaine, trimethylamine, glucose, fructose, mannose, starch or citrate. Sulfate, sulfite and thiosulfate were utilized as electron acceptors and elemental sulfur inhibited growth. Nitrate did not support growth. The novel isolate was capable of performing dismutation (inorganic fermentation); good growth, with optical density 0·2–0·25, was observed on sulfite (5 mM) or thiosulfate (10 mM) with 2 mM acetate. Sulfidogenesis was registered at thiosulfate dismutation (8 mM H2S) and at sulfite dismutation (3–4 mM H2S). Sulfate production was measured nephelometrically with BaCl2. Sulfate concentation was 8 mM during thiosulfate dismutation and 3·8 mM during sulfite dismutation; this stoichiometry is close to the dismutation data for Desulfovibrio sulfodismutans ThAc01T (Bak & Pfennig, 1987). Growth was inhibited by 5 mM molybdate, which blocks ATP sulfurylase in sulfate-reducing bacteria. Strain MLF1T was resistant to kanamycin and gentamicin (250 µg ml-1), as growth without morphological changes was observed, and sensitive to tetracycline (250 µg ml-1) and chloramphenicol (125 µg ml-1).
Fatty acids
Fatty acid methyl esters were extracted from fresh biomass grown for 5 days and identified by using the Microbial Identification system (MIDI) Moore Library of anaerobic bacteria. The major fatty acid methyl esters were (%): C14 : 0 (16·08); C16 : 1 (21·23); C18 : 0 (17·91); and a mixture of C18 unsaturated fatty acids in cis- and trans-configurations (19·80). In lower amounts were (%): C16 : 0 (11·54); C18 : 1 (10·61); and C18 : 2 (2·84).
DNA analysis
The G+C content of the genomic DNA of strain MLF1T was measured by the HPLC method as described previously (Mesbah et al., 1989). An Alltima C18 column [250x4·6 mm, 5 µm particle size (Alltech)] and 8 % (v/v) methanol were used in this study. The results reported are the mean of three determinations for each of two degradations of the DNA. The G+C content of the genomic DNA of strain MLF1T was 63·0±0·1 mol% (mean±standard deviation, n=6).
16S rRNA gene sequence analysis
Isolation of genomic DNA, amplification of the 16S rRNA gene and sequence determination were performed as described previously (Hoover et al., 2003). The quality of the consensus sequence was confirmed with data from eight different clones. The sequence of strain MLF1T was aligned with closely related sequences found in GenBank after a BLAST search (Altschul et al., 1990) by using the PileUp program from the GCG Wisconsin package. Pairwise distances were computed with MEGA version 2.0 (Kumar et al., 2001) by using the Jukes–Cantor (1969) model. An unrooted phylogenetic tree was constructed with the MEGA program by using the neighbour-joining method (Saitou & Nei, 1987). A sequence that covered 1481 nt of the 16S rRNA gene of strain MLF1T was obtained, corresponding to positions 28–1515 of the Escherichia coli 16S rRNA gene sequence. The G+C content of this sequence was 56·58 mol%. The sequence was compared with all sequences presently available in GenBank and appeared to be highly homologous to sequences from sulfate-reducing bacteria that belong to the 
-branch of the Proteobacteria. The phylogenetic tree, based on 1258 common nucleotide positions, shows that the closest relationship of strain MLF1T is to the genus Desulfonatronum, which is located between two large clusters that represent the genera Desulfovibrio and Desulfomicrobium (Fig. 2). The highest degree of relatedness of strain MLF1T was observed with Desulfonatronum lacustre Z-7951T. Pairwise comparison of the complete 16S rRNA gene sequences of strain MLF1T and Desulfonatronum lacustre Z-7951T showed only 97·6 % similarity over an alignment of 1359 nt.
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; Gillis et al., 1970). Purified genomic DNA (200 µg) from strain MLF1T and Desulfonatronum lacustre Z-7951T was sonicated to generate DNA fragments of 500–700 bp. Any residual RNA and single-stranded DNA was removed by treatment with RNase A and S1 nuclease, respectively (Ausubel et al., 1987). Concentration and purity of the DNA were determined from A260 readings and the ratio between A260 and A280 readings, by using a Shimadzu UV-160 spectrophotometer. DNA (80 µg) from each of these micro-organisms was then denatured in 1xSSC buffer (pH 7·0) by increasing the temperature of the sample from 26 to 100 °C (at a rate of 1 °C min-1) and A260 was recorded. The experiment was conducted in triplicate. The melting temperature (Tm) was determined by calculating the temperature at which the hyperchromicity reached half of the value obtained after complete melting. The Tm value of the genomic DNA of strain MLF1T was 71±2 °C (mean±standard deviation, n=3), whereas it was 63±2 °C for Desulfonatronum lacustre Z-7951T.
DNA–DNA hybridization
To determine the homology of genomic DNA between strain MLF1T and Desulfonatronum lacustre Z-7951T, DNA–DNA hybridization was performed by DNA reassociation kinetics as described previously (De Ley et al., 1970; Johnson, 1985). Purified, sonicated genomic DNA (80 µg) from each of these micro-organisms was added to 4xSSC buffer (pH 7·0) and 25 % deionized formamide. DNA was denaturated by raising the temperature to 100 °C and then cooled to 5 °C above their respective melting temperatures. Then the temperature was rapidly lowered (1·5 min) to the reassociation temperature and A270 was recorded at 5 s intervals for a total of 20 min. The initial reassociation kinetics were determined by linear regression analysis. The experiment was conducted in triplicate. The homology of the DNA from these two micro-organisms was calculated by using the equation described by De Ley et al. (1970). All statistical analyses were performed using Microsoft Excel software. DNA–DNA hybridization established 51 % homology between the genomes of strain MLF1T and Desulfonatronum lacustre Z-7951T.
Genome size
The genome sizes of strain MLF1T and Desulfonatronum lacustre Z-7951T were determined by using DNA reassociation kinetics, following the equation described by Gillis et al. (1970). The genome size for strain MLF1T was 1·6x109 Da, whereas that for Desulfonatronum lacustre Z-7951T was 2·1x109 Da.
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DISCUSSION |
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TOPABSTRACTMAIN TEXTDISCUSSIONREFERENCES |
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). In previous work, a study of anaerobic bacterial communities was performed on samples of equatorial soda Magadi Lake (Kenya) and central Asian Khadyn alkalic lake (Siberia). Our investigation dealt with the unique ecosystem of an ancient soda lake in California, which also has an athalassic nature. The novel isolate MLF1T is a typical secondary anaerobe, the main function of which in the bacterial anaerobic community is the consumption of hydrogen and low-molecular-mass end-products of primary anaerobes. Two novel primary anaerobes, ASpG1T and APOT, were also isolated from the same sample. Detailed study of these new isolates showed that they belonged to novel species: Spirochaeta americana sp. nov. (Hoover et al., 2003) and ‘Tindallia californiensis’ sp. nov. (Pikuta et al., 2003), respectively. In both cases, the closest relationships (with <1 % difference) were with the species Spirochaeta alkalica and Tindallia magadiensis, respectively, isolated from the alkaline anaerobic community of soda Lake Magadi (Zhilina et al., 1996; Kevbrin et al., 1998, 1999). It is interesting to note that the sulfate-reducer Desulfonatronovibrio hydrogenovorans Z-7935T, which was also isolated from Lake Magadi in Kenya (Zhilina et al., 1997), exhibited 10 % difference in 16S rDNA sequence from strain MLF1T. The most closely related species to strain MLF1T was Desulfonatronum lacustre Z-7951T, a sulfate-reducer from the alkaline anaerobic bacterial community of Khadyn Lake, central Asia. Notwithstanding the fact that strains MLF1T and Z-7951T have the same morphology and catabolism (an identical list of electron donors and electron acceptors), these strains have different physiologies and anabolisms: American strain MLF1T is an alkaliphile with dependence on NaCl and an autotrophic type of anabolism, but Asian strain Z-7951T is a lithoheterotroph that does not need NaCl in the growth medium. Also, analyses of DNA G+C content showed a significant difference between strain MLF1T and Z-7951T (>6 mol%). DNA–DNA hybridization of genomic DNA between strain MLF1T and Desulfonatronum lacustre Z-7951T exhibited 51 % homology. The melting temperature (Tm) of the genomic DNA of strain MLF1T was 8 °C higher than that of Desulfonatronum lacustre Z-7951T. Finally, there was a significant difference in the genome size between strain MLF1T and the closely related species Desulfonatronum lacustre Z-7951T. Comparison of these DNA data of strain MLF1T with those of the most closely related species, Desulfonatronum lacustre Z-7951T, indicates that there are sufficient differences for strain MLF1T to be considered as a separate species. In Table 1, comparative characteristics for all known alkaliphilic sulfate-reducers are provided.
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Description of Desulfonatronum thiodismutans sp. nov.
Desulfonatronum thiodismutans (thi.o.dis'mu.tans. Gr. thios sulfur; N.L. part. adj. dismutans dismutating, splitting; N.L. part. adj. thiodismutans sulfur-dismutating, pertaining to the ability of the organism to dismutate thiosulfate and sulfite).
Motile, vibrio-shaped cells with a single polar flagellum, 0·6–0·7x1·2–2·7 µm in size. Gram-negative. Non-spore-forming. Haloalkaliphilic: pH range for growth is 8·0–10·0, with optimum growth at pH 9·5. Growth is obligately dependent on Na+ and 
ions. Range of NaCl for growth is >1–7 % (w/v); optimum growth occurs at 3 % (w/v) NaCl. Mesophilic: temperature range for growth is 15–48 °C; optimum growth occurs at 37 °C. Cells can be stored frozen in liquid medium. Strictly anaerobic and catalase-negative. Does not grow without sulfate, which is used as an electron acceptor with H2S as the end product. Sulfite and thiosulfate are alternative electron acceptors, but sulfur and nitrate are not. Elemental sulfur and molybdate inhibit growth. Lithoheterotrophic, facultatively lithoautotrophic (slow growth on H2+CO2) and uses H2, formate and ethanol as electron donors. A supplement of vitamins is required and yeast extract stimulates growth. Capable of receiving energy by the dismutation of thiosulfate or sulfite (with 2 mM sodium acetate and carbonate as carbon sources). Resistant to kanamycin and gentamicin, but sensitive to tetracycline and chloramphenicol. Genomic DNA G+C content of the type strain is 63·0 mol% (HPLC). Major fatty acid methyl esters are C14 : 0, C16 : 1, C18 : 0 and a mixture of C18 unsaturated fatty acids.
The type strain is MLF1T (=DSM 14708T=ATCC BAA-395T). Isolated from mud sediments of alkaline, hypersaline, soda Mono Lake in California, North America.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Pikuta, E. V. & Hoover, R. B. (2001). Sulfate- and sulfur-reducing bacteria as terrestrial analogs for microbial life on Jupiter's satellite Io. In Instruments, Methods, and Missions for Astrobiology IV, Proceedings of SPIE Conference, vol. 4495, pp. 232–254. Edited by R. B. Hoover, G. V. Levin, R. R. Paepe & A. Y. Rozanov. San Diego: SPIE.
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