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1 Max-Planck-Institute for Marine Microbiology, Celsiusstr. 1, 28359 Bremen, Germany
2 University of Hamburg, Institute of Soil Science, Allende-Platz 2, 20146 Hamburg, Germany
Correspondence
Verona Vandieken
vvandiek{at}mpi-bremen.de
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Desulfotomaculum arcticum strain 15T is DQ148942.
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). Strains of the spore-forming genera Desulfotomaculum and Desulfosporosinus were isolated from cold sediments off the coast of Denmark (Isaksen et al., 1994), from permanently cold deep-sea sediments (Barnes et al., 1998) and from permafrost soil (Vainshtein et al., 1995), although these bacteria are not able to grow at in situ temperatures of those localities.
Strain 15T was isolated at 28 °C from sediment of Nordfjorden, Station BC (water depth 100 m, bottom water temperature 1·8 °C) on the west coast of Svalbard. The first enrichment culture was artificial sea-water medium (Widdel & Bak, 1992) with 28 mM sulfate and a suspension of lyophilized cyanobacteria (Spirulina) as carbon and energy source. For isolation in deep-agar dilution series, the Spirulina suspension was replaced by a fatty acid mixture of acetate, lactate, butyrate and propionate. The tests for physiological characterization were performed in duplicate in medium with a lower salt concentration (salt-water medium) (Widdel & Bak, 1992) at 37 °C. Cultures growing with alternative substrates were transferred into fresh test medium for verification. Temperature tolerance of the strains was determined in an aluminium temperature-gradient block at 13 different temperatures between 20 and 50 °C (Sagemann et al., 1998). The salt requirement was determined in media with 12 different NaCl concentrations between 0·05 and 5 % (w/v) and 10 different MgCl2.6H2O concentrations between 0·02 and 3·6 % (w/v). The pH optima of the strains were determined in media with 12 different pH values that covered a range from pH 5·5 to 8·8. For all tests, growth was monitored spectrophotometrically (UV 1202; Shimadzu) by measuring optical density at 580 nm.
PCR amplification of 16S rRNA gene was performed with the primers 8F and 1492R, and the PCR product was amplified for sequence analysis with primers 8F, 341F, 518F, 534R, 1099F and 1492R (Buchholz-Cleven et al., 1997). The phylogenetic position was evaluated by the ARB program package (Ludwig et al., 2004) using the neighbour-joining, maximum-likelihood and maximum-parsimony algorithms with different sets of filters. Positions 109–1387 (Escherichia coli numbering) were used for analyses, as regions that either exhibited alignment uncertainties or were not sequenced were excluded.
Cells of strain 15T were rods, 2–3x1 µm in size and, when endospores were formed, cells appeared lemon-shaped (Fig. 1). Endospores were spherical and located in the centre of the cells. Motility was not observed under the culture conditions used. Gram staining was negative. A negative Gram stain has been repeatedly described for species of Desulfotomaculum, yet the ultrastructure of the cell wall of these species, examined by electron microscopy, is usually typical for Gram-positive bacteria (Stackebrandt et al., 1997); this was not tested for strain 15T.
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The pH optimum of strain 15T was 7·1–7·5 and growth occurred over the range of pH 6·8–7·5. The strain grew at NaCl concentrations of 0·05–4·5 % and best at 1–1·5 %; the optimum concentration for MgCl2.6H2O was 0·4 % and the growth range was 0·4–2·5 %. Optimum growth of strain 15T occurred at 44 °C and growth was observed between 26 and 46·5 °C. Strain 15T did not grow at 4, 10, 20 or 25 °C. The growth rate of strain 15T with sulfate and lactate at 41 °C was 0·046 h–1. Cells of strain 15T contained MK-7 as sole menaquinone, as determined by the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany. The DNA G+C content was 48·9 mol% (determined by the DSMZ).
Strain 15T was closely related to Desulfotomaculum thermosapovorans (93·5 % 16S rRNA gene sequence similarity), Desulfotomaculum sapomandens (93·4 %), Desulfotomaculum gibsoniae (93·3 %) and Desulfotomaculum geothermicum (93·2 %) (Fig. 2), and shares important physiological characteristics with these species (Table 1). These include the usage of sulfate, sulfite and thiosulfate as electron acceptors and formate, hydrogen, butyrate, ethanol, butanol, propanol, malate, fumarate and pyruvate as electron donors (Cord-Ruwisch & Garcia, 1985; Daumas et al., 1988; Fardeau et al., 1995; Kuever et al., 1999). The species are easily distinguished by their differences in temperature tolerance and usage of other electron donors and acceptors (Table 1).
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). This bacterium was described as having a significantly lower temperature optimum for growth (20–30 °C) than our novel strain 15T (44 °C). However, the authors did not test for growth at in situ temperatures and today the strain is considered as lost (Stackebrandt et al., 1997). Due to the moderately thermophilic growth range, 26–46·5 °C, strain 15T apparently could not multiply at in situ temperatures of permanently cold Arctic sediments, where the temperature never exceeds 4 °C. During laboratory experiments with fjord sediments of Svalbard, sulfate reduction in the thermophilic temperature range (40–60 °C) has been observed (M. Nickel, personal communication). The experiments showed that sulfate reduction rates of fresh and pasteurized sediment exceed the in situ rates after a lag phase of 24 h (probably due to the germination of spores). This suggests that our isolate belongs to a significant number of thermophilic sulfate-reducing bacteria present as spores in the sediments. In cold sediments of Aarhus Bay (Denmark), thermophilic populations of sulfate-reducing and aerobic respiring bacteria have been found with optimum temperatures for thermophilic sulfate reduction of 60 °C and for aerobic respiration of 55 °C (Isaksen et al., 1994; Thamdrup et al., 1998). From most probable number enumeration at 60 °C with propionate, a population density of thermophilic sulfate reducers of 2·8x104 cells cm–3 for the Aarhus Bay sediment was estimated and a thermophilic spore-forming bacterium with similarities to Desulfotomaculum kuznetsovii was isolated (Isaksen et al., 1994). Aerobic and sulfate-reducing, spore-forming bacteria with minimum growth temperatures considerably above in situ temperatures have been isolated from permanently cold habitats, such as deep-sea sediments and permafrost soil (Bartholomew & Paik, 1966; Barnes et al., 1998; Vainshtein et al., 1995). The origin of the different thermophilic populations have been proposed to be geothermal environments or anthropogenic sources from which the spores were dispersed by wind or terrestrial river run-off (Bartholomew & Paik, 1966; Isaksen et al., 1994; Thamdrup et al., 1998). We do not know the growth habitat of our isolates.
Description of Desulfotomaculum arcticum sp. nov.
Desulfotomaculum arcticum (arc'ti.cum. L. neut. adj. arcticum from the Arctic, referring to the place where the type strain was isolated).
Cells are rod-shaped, endospore-forming, 2–3x1 µm in size, strictly anaerobic. No vitamins are required for growth. Sulfate, thiosulfate and sulfite serve as electron acceptors. Oxidation of hydrogen, formate, lactate, propionate, butyrate, hexanoate, methanol, ethanol, propanol, butanol, pyruvate, malate, succinate, fumarate, proline, alanine and glycine occurs in the presence of sulfate. Ferments pyruvate. pH range of growth is 6·8–7·5, optimum pH 7·1–7·5. Temperature range for growth is 26–46·5 °C, optimum temperature 44 °C. The DNA G+C content is 48·9 mol%.
The type strain, strain 15T (=DSM 17038T=JCM 12923T), was isolated from a permanently cold fjord sediment of Svalbard.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Bartholomew, J. W. & Paik, G. (1966). Isolation and identification of obligate thermophilic sporeforming bacilli from ocean basin cores. J Bacteriol 92, 635–638.
Buchholz-Cleven, B. E. E., Rattunde, B. & Straub, K. L. (1997). Screening for genetic diversity of isolates of anaerobic Fe(II)-oxidizing bacteria using DGGE and whole-cell hybridization. Syst Appl Microbiol 20, 301–309.
Cord-Ruwisch, R. & Garcia, J.-L. (1985). Isolation and characterization of an anaerobic benzoate-degrading spore-forming sulfate-reducing bacterium, Desulfotomaculum sapomandens sp. nov. FEMS Microbiol Lett 29, 325–330.[CrossRef]
Daumas, S., Cord-Ruwisch, R. & Garcia, J.-L. (1988). Desulfotomaculum geothermicum sp. nov., a thermophilic, fatty acid-degrading, sulfate-reducing bacterium isolated with H2 from geothermal ground water. Antonie van Leeuwenhoek 54, 165–178.[CrossRef][Medline]
Fardeau, M.-L., Ollivier, B., Patel, B. K. C., Dwivedi, P., Ragot, M. & Garcia, J.-L. (1995). Isolation and characterization of a thermophilic sulfate-reducing bacterium, Desulfotomaculum thermosapovorans sp. nov. Int J Syst Bacteriol 45, 218–221.
Iizuka, H., Okazaki, H. & Seto, N. (1969). A new sulfate-reducing bacterium isolated from Antarctica. J Gen Appl Microbiol 15, 11–18.
Isaksen, M. F., Bak, F. & Jørgensen, B. B. (1994). Thermophilic sulfate-reducing bacteria in cold marine sediments. FEMS Microbiol Ecol 14, 1–8.
Kuever, J., Rainey, F. A. & Hippe, H. (1999). Description of Desulfotomaculum sp. Groll as Desulfotomaculum gibsoniae sp. nov. Int J Syst Bacteriol 49, 1801–1808.
Ludwig, W., Strunk, O., Westram, R. & 29 other authors (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32, 1363–1371.
Sagemann, J., Jørgensen, B. B. & Greef, O. (1998). Temperature dependence and rates of sulfate reduction in cold sediments of Svalbard, Arctic Ocean. Geomicrobiol J 15, 85–100.
Stackebrandt, E., Sproer, C., Rainey, F. A., Burghardt, J., Päuker, O. & Hippe, H. (1997). Phylogenetic analysis of the genus Desulfotomaculum: evidence for the misclassification of Desulfotomaculum guttoideum and description of Desulfotomaculum orientis as Desulfosporosinus orientis gen. nov., comb. nov. Int J Syst Bacteriol 47, 1134–1139.
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Thamdrup, B., Hansen, J. W. & Jørgensen, B. B. (1998). Temperature dependence of aerobic respiration in a coastal sediment. FEMS Microbiol Ecol 25, 189–200.[CrossRef]
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Widdel, F. & Bak, F. (1992). Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes, pp. 3352–3378. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K. H. Schleifer. New York: Springer.
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