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Department of Microbial Ecology, Bldg 540, Institute of Biological Sciences, University of Aarhus, 8000 Aarhus C, Denmark
Correspondence
Kai Finster
Kai.Finster{at}biology.au.dk
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 28 November 2003 as DOI 10.1099/ije.0.02820-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA and partial DSR gene sequences of strain P2T are AY268891 and AY268892.
Phase-contrast micrographs showing cells of strain P2T and a DSR sequence-based phylogenetic tree are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Despite its importance, in situ concentrations of propionate are low, because it is efficiently consumed by sulfate-reducing bacteria. Until recently, all propionate-consuming sulfate reducers grouped in one phylogenetic lineage around the genus Desulfobulbus (Widdel & Pfennig, 1982; Isaksen & Teske, 1996; Rabus et al., 2000). Apart from a common phylogeny, the organisms also all oxidize propionate incompletely to acetate. However, within the past few years, two novel species of propionate-consuming sulfate reducers have been isolated that share with the ‘Desulfobulbaceae’ the incomplete oxidation of propionate but group phylogenetically with the completely oxidizing genera of the Desulfonema/Desulfococcus/Desulfosarcina assemblage. The two species were placed in different genera as Desulfofaba gelida and Desulfomusa hansenii (Knoblauch et al., 1999; Finster et al., 2001). In this communication, we report on the isolation and characterization of a third isolate, designated strain P2T, which shares a common phylogeny and physiology with both Desulfofaba gelida and Desulfomusa hansenii.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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and the temperature was 6·3 °C. The sediment consisted of fine sand, silt and clay. Measurements of methane oxidation rates and sulfate reduction revealed that both rates peaked in the 170–200 cm depth interval. This zone was identified as the sulfate–methane transition zone. Sediment for enrichment cultures was withdrawn from that depth.
Enrichment and isolation.
The enrichment medium was identical to DSMZ medium 193 with the following modifications. Firstly, sodium acetate solution was not added and, secondly, the vitamin solution used in the original medium was replaced by the following solutions: 1 ml vitamin solution (10 mg biotin, 3 mg folic acid, 15 mg pyridoxine hydrochloride dihydrate, 100 mg nicotinic acid, 50 mg calcium D-pantothenate, 40 mg p-aminobenzoic acid and 1·42 g Na2HPO4 dissolved in 1 l distilled water), 1 ml thiamin chloride solution (100 mg thiamin chloride and 3·56 g Na2HPO4 dissolved in 1 l distilled water) and 1 ml vitamin B12 solution (50 mg cyanocobalamin dissolved in 1 l distilled water). In addition, 2 ml Na2SeO3.5H2O solution (stock concentration 10 µM) and 2 ml Na2WO4 solution (stock concentration 10 µM) were added to 1 l medium. The medium was prepared as described in the DSMZ manual. The medium was distributed into 50-ml screw-capped bottles. CaCl2 (10 mM final concentration), MgCl2 (50 mM final concentration), propionate (15 mM final concentration) and sulfate (20 mM final concentration) were added from sterile stock solutions prior to inoculation. For the isolation of pure cultures, the modified deep agar dilution technique (Isaksen & Teske, 1996) was applied. The agar was washed three times in distilled water before use.
Physiological tests.
Substrate utilization was studied in completely filled screw-capped bottles (50 ml) or Hungate tubes with a gas phase. Growth tests with CO and methane were performed in half-full 100-ml bottles sealed with butyl-rubber stoppers. Growth was determined microscopically and by following the production of hydrogen sulfide using the method of Cline (1969). Cultures showing growth were transferred to fresh medium containing the respective substrate at least three times to confirm the result. Cultures not showing growth after 1 month were maintained for at least 4 months and checked for growth on a regular basis. The presence of polyhydroxyalkanoates in the cells was investigated with the Nile blue stain (Ostle & Holt, 1982). Temperature experiments were carried out in duplicate in a temperature-controlled block at 11 different temperatures ranging from 8·8 to 37·4 °C. pH tolerance was tested in triplicate in media adjusted to 12 different pH values between 4·0 and 8·5. Growth rates were calculated from changes in OD600. At pH values above 7·4, reliable OD measurements were no longer possible due to precipitation of medium components. Production of hydrogen sulfide was therefore measured in all tubes and used as an indicator of activity. Cell production was confirmed by microscopy with a non-growing control as reference. The salt requirement for growth was monitored at 11 different NaCl concentrations ranging from 6 to 38 g l-1, eight different MgCl2.6H2O concentrations ranging from 5 to 68 mM and eight different CaCl2.2H2O concentrations ranging from 1 to 13 mM. Tests were carried out in duplicate. The effect of different salt concentrations was monitored by measuring H2S production over time.
Chemical analyses.
Sulfide was measured as described by Cline (1969). Sulfate was determined by suppressed ion chromatography according to Isaksen & Finster (1996). Propionate and acetate were analysed by ion-exclusion chromatography as described by Finster et al. (2001). The G+C content of genomic DNA was determined at the Identification Service of the DSMZ by Peter Schumann. DNA was isolated according to Visuvanathan et al. (1989) and purified as described by Cashion et al. (1977) and the G+C content was determined by HPLC analysis (Mesbah et al., 1989; Tamaoka & Komagata, 1984).
Microscopy.
Samples for TEM were placed on a carbon-celloidin copper grid (200 mesh) and stained with a drop of 1 % (w/v) uranyl acetate. Cells were observed with a JEOL 1200EX transmission electron microscope at 120 kV.
Nucleic acid extraction, PCR amplification and sequencing.
Nucleic acid was extracted using the FastDNA spin kit for various samples (Bio 101) according to the instructions of the manufacturer. The SSU rDNA was PCR-amplified and sequenced as described by Lane (1991). Almost complete 16S rDNA sequences were obtained with primers 26F/1390R (primer nomenclature refers to the 5'-ends of respective target sites on the 16S rDNA according to the Escherichia coli numbering of the 16S rRNA; Brosius et al., 1981). PCR was performed at an annealing temperature of 57 °C with 25 cycles. PCR products were purified with the QIAquick PCR purification kit (Qiagen) according to the instructions of the manufacturer. Sequences were determined using the direct dideoxyribonucleotide chain-termination method with reverse transcriptase as described by Lane et al. (1985) using the kit from Amersham Pharmacia Biotech. The gel was run on an ALFexpress sequencer (Amersham Pharmacia Biotech) and sequences were handled with the ALFwin software (Amersham Pharmacia Biotech). A sequence of 1386 nucleotides was obtained after sequencing both strands with multiple primers.
The dissimilatory sulfite reductase (DSR) gene was amplified using primers designed by Wagner et al. (1998). Due to problems with non-specific annealing and low yields of the correct amplicon, the band of the correct length was cut out of an agarose gel and purified (QIAquick gel extraction kit; Qiagen) following the manufacturer's instructions. The DNA was ligated into a pCR-XL-TOPO vector and transformed into ONE SHOT E. coli cells according to the instructions of the manufacturer (TOPO-XL-pCR Cloning; Invitrogen); randomly selected clones were purified using a purification kit (QIAprep Spin Miniprep kit; Qiagen). Clones were amplified using a ThermoSequenase fluorescent cycle-sequencing kit (Amersham Pharmacia Biotech) and sequenced on an ALFexpress sequencer. A partial sequence of 876 nucleotides was obtained; 845 positions were used in the alignment.
Phylogenetic analysis.
Sequence fragments were assembled manually in SEQPUP version 0.6 (Gilbert, 2002). Each resulting rDNA sequence was aligned with its closest relative using the on-line service of Ribosomal Database Project II (RDP-II) Sequence Aligner version 1.7 and compared to the GenBank and RDP-II databases using the BLAST algorithm (national center for biotechnology information) and SEQUENCE MATCH version 2.7 (Maidak et al., 2001; Wheeler et al., 2002; Zhang et al., 2000). Alignments were checked manually in SEQPUP. DSR gene sequences were aligned as nucleotide sequences or translated into an amino acid sequence before being aligned against their closest relatives. Phylogenetic analyses were performed with PAUP version 4.0b10. Only unambiguously aligned positions were used. The data matrix for the 16S rDNA sequences was analysed by distance-matrix (neighbour-joining), maximum-parsimony and maximum-likelihood approaches, whereas the DSR matrices were analysed by distance-matrix analysis only. Generally, bootstrap analysis was performed with 100 resamplings, except from the distance and maximum-parsimony algorithms analysing the relatedness of the SSU rRNA genes. Here, 1000 bootstraps were performed. Multifurcations were created at the appropriate basal node when branching patterns were only supported in less than 50 % of the bootstrap resamplings.
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RESULTS AND DISCUSSION |
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Purity controls
Culture purity was checked microscopically prior to each transfer. In addition, purity of the isolate was tested in sulfate-free medium containing yeast extract (0·1 %, w/v), glucose (10 mM), fumarate (10 mM) and pyruvate (20 mM). There was no growth on this medium.
Cell morphology
Cells of strain P2T were slightly curved, rod-shaped with round ends. They were 0·8–1·0 µm wide and 3–3·8 µm long (Fig. 1, Table 1). When grown with thiosulfate as electron acceptor, cells were longer than cells grown with sulfate as electron acceptor (Supplementary Figs A and B in IJSEM Online). Cells were motile by means of a single polar flagellum.
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-subclass of the Proteobacteria. Phylogenetic analysis of 16S rDNA (Fig. 2) and the DSR gene sequence (Supplementary Fig. C) showed that strain P2T is related to the Desulfonema/Desulfococcus/Desulfosarcina assemblage, which also includes the incompletely oxidizing genera ‘Desulfobotulus’, Desulfofaba, Desulfomusa and Desulforegula. The overall branching pattern was supported by high bootstrap values in trees based on neighbour-joining, maximum-parsimony and maximum-likelihood algorithms. The closest relatives of strain P2T were Desulfofaba gelida and Desulfomusa hansenii, with respective 16S rDNA sequence similarity of 92·9 and 91·5 %. The detailed branching pattern was, however, dependent on the algorithm. Using the maximum-likelihood algorithm, strain P2T formed a common line of descent with Desulfofaba gelida and Desulfomusa hansenii. The branching pattern was supported by a bootstrap value of 54 %. Interestingly, neither the neighbour-joining nor maximum-parsimony algorithm supported this branching pattern. In contrast, both algorithms supported a multifurcation as the best fit, indicating that a common ancestor of strain P2T, Desulfomusa hansenii and Desulfofaba gelida could not be assigned.
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. The optimal pH for growth was 6·8–7·1. The strain was able to grow in the pH range 6·0–7·75. The strain was grown at a salinity of 13·5 g l-1; optimal growth was obtained in the range 10–16 g l-1. However, the strain was able to grow at all salinities tested (6–38 g l-1). CaCl2 at a concentration of 7 mM enhanced growth and, again, growth was observed at all tested CaCl2 concentrations (1–13 mM). MgCl2 concentrations of 5–68 mM neither enhanced nor inhibited growth. The temperature range for growth was 5–33 °C. The isolate grew optimally at 28 °C with a doubling time of 4·3 h. With sulfate as electron acceptor, the isolate grew with propionate, lactate or 1-propanol as electron donors. Sulfate, sulfite and thiosulfate served as electron acceptors, while sulfur, nitrate, iron(III) citrate and fumarate did not. The strain also grew by fermentation of lactate. In contrast to Desulfomusa hansenii and Desulfofaba gelida, strain P2T is not very versatile with respect to its range of substrates (Table 1). Strain P2T did not grow on pyruvate, succinate, fumarate, ethanol, butanol or alanine, substrates upon which Desulfomusa hansenii and Desulfofaba gelida grow. However, strain P2T and Desulfofaba gelida but not Desulfomusa hansenii grow with thiosulfate as electron acceptor. In the assemblage of its closest relatives (‘Desulfobotulus’, Desulfofrigus, Desulfomusa and Desulfofaba), strain P2T is distinct in its ability to ferment lactate, but fermentation in general is known from several members of the assemblage (Widdel & Pfennig, 1984; Devereux et al., 1989; Knoblauch et al., 1999). The three strains Desulfomusa hansenii DSM 12642T, Desulfofaba gelida DSM 12344T and strain P2T were isolated from different habitats: Desulfomusa hansenii is a mesophilic bacterium isolated from the interior of surface-sterilized eelgrass roots, Desulfofaba gelida is a psychrophilic bacterium isolated from polar surface sediment and strain P2T is a mesophilic bacterium isolated from the methane–sulfate transition zone 1·5 m below the sediment surface. Thus, we have evidence that anaerobic propionate degradation in sulfate-containing habitats is accomplished by at least two phylogenetically distinct lines of descent. Future studies should focus on the quantitative importance of the two lines in nature.
Storage compounds
Strain P2T accumulated polyhydroxyalkanoates; cells of strain P2T and Desulfomusa hansenii contained inclusions of polyhydroxyalkanoates of an unidentified type (K. Finster, unpublished data). Desulfofaba gelida was not tested for these compounds. The physiological role of these storage compounds has not been determined so far. The presence of polyhydroxyalkanoates, however, distinguishes them from Desulfobulbus species, which accumulate polyglucose instead (Stams et al., 1983).
Stoichiometry of propionate oxidation
Changes in concentrations of propionate, acetate, sulfate and hydrogen sulfide and in the amount of cell carbon were measured in three different cultures. Propionate was oxidized incompletely to acetate and CO2. One mol acetate was formed from 1 mol propionate and 1 mol hydrogen sulfide was formed from 1 mol sulfate. The molar ratios of propionate dissimilation to acetate and sulfide production agreed with the following equation:
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The amount of propionate consumed for cell material synthesis was calculated by the equation given by Finster et al. (2001): 
. Thus, 0·0118 mmol propionate is needed for production of 1·0 mg cells (dry weight). Strain P2T produced 2·60 g biomass per mol propionate and thus incorporated about 3 % of the consumed propionate into biomass. The inability of strain P2T to oxidize acetate completely to CO2 is interesting, considering its phylogenetic affiliation to the complete oxidizers such as Desulfonema, Desulfococcus and Desulfosarcina. Until recently, incompletely oxidizing sulfate reducers grouped separately from the complete oxidizers, with only one exception, ‘Desulfobotulus sapovorans’ (=[Desulfovibrio] sapovorans) (Devereux et al., 1989, 1990). In 1999, however, two incomplete sulfate reducers, Desulfofaba gelida and Desulfofrigus fragile, whose closest relatives were members of the Desulfosarcina group, were isolated. In 2001, two additional incompletely oxidizing sulfate reducers, Desulfomusa hansenii and Desulforegula conservatrix, were described that were affiliated with the Desulfosarcina group (Finster et al., 2001; Rees & Patel, 2001). The affiliation of incomplete oxidizers to the complete oxidizers is interesting, because the pathway used for degradation of the organic substrates differs markedly.
The completely oxidizing sulfate reducers use the classical 
-oxidation pathway to degrade fatty acids (Janssen & Schink, 1995a, b). The oxidation of organic substrates by the incomplete oxidizer Desulfobulbus propionicus follows the reverse methylmalonyl-CoA pathway (Kremer & Hansen, 1988). Preliminary data indicate that Desulfomusa hansenii and strain P2T use the same pathway as Desulfobulbus propionicus. Thus, despite the phylogenetic distance (Fig. 2), the pathway of propionate degradation seems to be shared among propionate-degrading sulfate reducers.
Taxonomic conclusions
We propose that strain P2T (=DSM 15249T=ATCC BAA-815T) represents a novel species of the genus Desulfofaba, Desulfofaba fastidiosa sp. nov. In addition, based on its close phylogenetic affiliation to Desulfofaba gelida (Fig. 2) and the phenotypic similarities, we propose to reclassify Desulfomusa hansenii as Desulfofaba hansenii comb. nov. The description of the genus Desulfofaba must also be amended.
Emended description of the genus Desulfofaba Knoblauch et al. 1999
The original description of this genus was provided by Knoblauch et al. (1999). Additionally, some species are able to produce inclusions of polyhydroxyalkanoates. The type species is Desulfofaba gelida.
Description of Desulfofaba hansenii comb. nov.
Basonym: Desulfomusa hansenii Finster et al. 2001.
The description of this taxon was provided by Finster et al. (2001). The type strain is P1T=DSM 12642T=ATCC 700811T.
Description of Desulfofaba fastidiosa sp. nov.
Desulfofaba fastidiosa (fas.ti.di.o'sa. L. fem. adj. fastidiosa fastidious, difficult to please, referring to the limited number of substrates used by the type strain).
Cells are curved, bean-shaped rods, 3–3·8 µm long and 0·8–1·0 µm wide when grown with sulfate, but longer when grown with thiosulfate. Cells are motile and have a single polar flagellum. Spores are not observed. Anaerobic growth with propionate, lactate or 1-propanol as electron donors and sulfate, sulfite or thiosulfate as electron acceptors. Growth is also possible by fermentation of lactate. The pH range for growth is 6·0–7·75 (optimum 6·8–7·1). Temperature range for growth is 5–33 °C (optimum 28 °C). The DNA G+C content of the type strain is 48·8 mol%.
The type strain, P2T (=DSM 15249T=ATCC BAA-815T), was isolated from the sulfate–methane transition zone (1·5 m below sediment surface) of Aarhus Bay (Denmark).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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