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Department of Microbiology, Institute of Biological Sciences, University of Aarhus, Denmark
Correspondence
Kjeld Ingvorsen
kjeld.ingvorsen{at}biology.au.dk
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, dsrAB and apsA gene sequences of strain RT2T are AY649785, AY864856 and AY744465, respectively.
A transmission electron photomicrograph of a cell of strain RT2T grown on lactate with sulphate as the electron acceptor and consensus trees showing the phylogenetic affiliations of the DsrAB and ApsA amino acid sequences of strain RT2T are available as supplementary material in IJSEM Online.
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). The micro-organisms that have been most extensively studied in relation to MIC are sulphate-reducing bacteria (SRB) (Hamilton, 1998). MIC caused by SRB has been attributed mainly to the production of corrosive hydrogen sulphide and cathode depolarization, enhanced by their consumption of chemically produced hydrogen (Hamilton, 1985, 2003). Among SRB, Desulfovibrio species efficiently utilize hydrogen (Widdel & Bak, 1992; Peck, 1993). Consequently, MIC is commonly attributed to members of this genus (Rao et al., 2000; Pak et al., 2003; Pankhania, 1988). Recently, two novel Desulfovibrio strains were isolated that reportedly were capable of using metallic iron as the sole electron donor for the dissimilatory reduction of sulphate, in a process in which hydrogen does not act as an intermediate electron carrier (Dinh et al., 2004). The isolation of these two strains thus suggested a novel and more direct mechanism of MIC than that involving consumption of cathodic hydrogen. In many Danish cities, district heating systems work by circulating hot water to and from a heating plant to houses in a closed piping network. In order to prevent both chemical corrosion and growth of micro-organisms, the circulating water is regularly treated by deaeration, reverse osmosis and sodium hydroxide amendment, thereby maintaining anoxic, nutrient-poor and alkaline conditions in the system (Goeres et al., 1998). Despite these measures, total bacterial counts of around 105 cells per ml district heating water have been reported in waters of various Danish district heating systems, some of which have been exposed to MIC (Kjellerup et al., 2003). The presence of SRB has been demonstrated in several Danish district heating systems; however, their identity and their physiology were not investigated (Kjellerup et al., 2003, 2005). Although SRB thrive in a broad range of environments, only a few species, representing the genera Desulfonatronovibrio and Desulfonatronum, are obligately alkaliphilic. Some of these bacteria are able to grow at pH values >10 and not below pH 7.0 (Zhilina et al., 1997, 2005; Pikuta et al., 1998, 2003). In addition, a moderately alkaliphilic species with a growth range between pH 8.0 and 9.2 is known within the genus Desulfotomaculum (Pikuta et al., 2000). However, to date alkalitolerant members of the environmentally widely distributed genus Desulfovibrio have not been described. This paper describes the first reported characterization of an alkalitolerant SRB (strain RT2T), affiliated to the genus Desulfovibrio.
Strain RT2T was isolated from biofilms growing in the alkaline waters of a Danish district heating system where corrosion of the pipes had occurred. The biofilm samples were harvested from mild steel coupons (6.0x2.4 cm), which had been incubated for 4 months in a rotortorque reactor connected to the return line of the district heating system in Skanderborg (Jutland, Denmark). Typical characteristics of the return-line water were as follows: conductivity (<25 µS cm–1), sulphate (<20 µM), chloride ions (<750 µM), total inorganic nitrogen (<300 µM) and pH (9.5–10). The temperature of the anoxic return-line water was approximately 40 °C. Most of the biofilm was aseptically scraped off the steel coupons for use in other investigations (K. U. Kjeldsen, B. V. Kjellerup, K. Egli, B. Frølund, P. H. Nielsen and K. Ingvorsen, unpublished data) and the coupons were subsequently transferred to modified anoxic Widdel and Bak medium (Widdel & Bak, 1992) for enrichment of SRB. The modified medium (CM medium) comprised [g (l Milli-Q water)–1]: NaCl, 1.0; MgCl2.6H2O, 0.1; CaCl2.2H2O, 0.05; Na2SO4, 2.0 (4.0 after initial enrichments); NH4Cl, 0.25; KH2PO4, 0.1; KCl, 0.5; yeast extract (IDG) 0.5; CAPSO [3-(cyclohexylamino)-2-hydroxy-1-propansulphonic acid, pKa=9.4, 37 °C], 11.85. In addition, 1 ml trace mineral solution l–1 (Ingvorsen & Jørgensen, 1984) and 1 ml selenite-tungstate solution l–1 (Widdel & Bak, 1992) were added. The final pH of the medium was adjusted to 9.0 (after sterilization by autoclaving) using sterile NaOH. For the initial enrichment of SRB, a mixture of glucose, pyruvate, lactate, propionate and acetate (2 mM final concentration of each added substrate) was added to the CM medium from sterile anoxic stock solutions. The enrichments were incubated at 40 °C in the dark. After approximately 1 month of incubation of the mild steel coupons in CM medium, turbidity and sulphide production were observed in some enrichment cultures. Strain RT2T was isolated from one of these enrichments by repeated (three times) application of the roll-tube dilution technique (Hungate, 1976) using CM medium supplemented with hydrogen (0.6 atm. in headspace), acetate (20 mM), thiosulphate (20 mM) and agar (2 %, w/v). The purity of the culture was checked using phase-contrast microscopy at regular intervals. In addition, the purity of the isolate was tested by microscopy after incubation in sulphate-free CM medium (pH 7.5 or 9.0) containing yeast extract (0.15 %, w/v), glucose (10 mM) and pyruvate (20 mM). Aerobic growth was tested on nutrient broth (Scharlau Chemie) agar plates. Colonies of strain RT2T were disc-shaped and black, with a diameter of approximately 1 mm. In sulphate-containing CM medium, the cells were rod-shaped and slightly curved (1.4–1.9 µm long and 0.5–0.8 µm wide), whereas thiosulphate-grown cells appeared to be slightly wider. Dividing cells often occurred in chains. Spores were never observed. Transmission electron micrographs were obtained as described previously (Abildgaard et al., 2004). These demonstrated the presence of a single polar flagellum, which was up to 3.5 times the length of the cells of strain RT2T (see Supplementary Fig. S1 in IJSEM Online).
Growth tests were performed in CM medium adjusted to pH 9.0 (unless otherwise noted) in 16x125 mm Hungate anaerobic culture tubes (Bellco Glass) with 3 ml gas phase (nitrogen). Incubations were routinely carried out at 40 °C in the dark. Growth was evaluated microscopically, by measuring the OD600 directly in the tubes using a Novaspec II spectrophotometer (Pharmacia Biotech) fitted with a tube adaptor, and by following the production of sulphide using the method of Cline (1969). All substrate utilization experiments were performed in duplicate. Cultures were transferred to fresh medium at least three times to confirm the results. Incubations were maintained for at least 3 months and checked for growth on a regular basis. Electron acceptor utilization tests were done in sulphate-free CM medium supplemented with lactate (20 mM). The ability to utilize metallic iron as a growth substrate was tested in modified CM medium (pH 9.0) containing a low concentration of sulphate (4 mM), sterile mild steel coupons, yeast extract (0.05 %, w/v) and acetate (1 mM final concentration). Separate control incubations with and without yeast extract, acetate and mild steel coupons were also performed. In addition, the sulphate-reducing activity in the various types of incubation was measured by using the sensitive 35S-tracer technique with the single-step chromium reduction method to recover reduced sulphur species (Fossing & Jørgensen, 1989). Tracer incubations were initiated by injecting carrier-free 
(Isotope Laboratory, Risø, Denmark) at a final activity of 26 kBq (ml culture)–1 and then incubated at 40 °C for 27 days. Subsamples (1.0 ml) from the tracer incubations were removed with a syringe and mixed with a zinc acetate solution (20 %, w/v) to stop the biological activity and preserve the 35S-sulphides produced. The 35S activity was determined by liquid scintillation counting (Packard TRI-CARB 2900TR). Temperature, pH and NaCl experiments were carried out using lactate (20 mM) as electron donor and sulphate as electron acceptor. Temperature experiments were performed simultaneously (in duplicate) at 21 temperatures ranging from 7.3 to 54.3 °C using a temperature gradient block (Elsgaard et al., 1994). The pH tolerance was tested in triplicate at pH values ranging from 6.4 to 10.8. The pH of the medium was measured once a day throughout these experiments. In media adjusted to initial pH values below 7.5, the pH slowly increased during incubation and therefore the growth rates in these incubations were estimated from the initial part of the growth curves. The pH tolerance was further tested in duplicate incubations at six pH values ranging from 9.7 to 10.3. The pH of the medium was measured twice a day and adjusted if necessary during these incubations. Growing cultures were retransferred to fresh medium of the same pH to confirm the results. At pH values above 9.8, some precipitation of medium components occurred. However, it was still possible to distinguish between cell growth and precipitation by reference to a substrate-free control and by measuring sulphide concentrations. The salt requirement for growth was tested in duplicate at 12 NaCl concentrations ranging from approximately 0.8 to 10.0 g l–1. Strain RT2T grew between 16 and 47 °C (optimum growth temperature, 43 °C; doubling time, 
4 h) using lactate and sulphate (20 mM each) in media at a pH of 9.0 and 0.13 % (w/v) NaCl. The strain was able to grow at pH values ranging from 6.9 to 9.9, with an optimum pH for growth of 9.0–9.4 (Fig. 1). The strain grew at NaCl concentrations ranging from 0.085 to 0.7 % (w/v). With sulphate as electron acceptor, strain RT2T grew with lactate (10 mM), pyruvate (10 mM), formate (15 mM) and hydrogen/acetate (5 mM). No growth in the presence of sulphate was observed with propionate (10 mM), fumarate (10 mM), malate (10 mM), acetate (10 mM), benzoate (10 mM), butyrate (5 mM), citrate (10 mM), succinate (10 mM), oxamate (10 mM), fructose (5 mM), galactose (5 mM), glucose (5 mM), lactose (5 mM), maltose (5 mM), raffinose (5 mM), sucrose (5 mM), xylose (5 mM), glycerol (10 mM), choline (5 mM), ethanol (10 mM), methanol (10 mM), butanol (10 mM) or propanol (10 mM). Yeast extract was required for growth. When strain RT2T was incubated in medium containing yeast extract (0.05 %, w/v), acetate and mild steel coupons, consistent blackening of the medium occurred during eight consecutive transfers. However, microscopy revealed no more than a few free-living cells in these subcultures and only extremely low sulphate reduction rates (<1 µM day–1) were detected with the 35S radiotracer experiments. Thus, the mild steel coupons (i.e. Fe0) probably did not serve as an efficient electron donor for strain RT2T. In addition to sulphate, thiosulphate (10 mM) and sulphite (5 mM) could be utilized as electron acceptors using lactate as electron donor. Nitrate (2 mM), elemental sulphur (approx. 20 g l–1) and ferric iron [10 mM; added from a FeCl3 solution of neutral pH prepared according to Lovley (2000)] did not support growth of strain RT2T using lactate as electron donor in sulphate-free medium. Strain RT2T was able to ferment pyruvate (20 mM), but not lactate (20 mM) or fumarate (20 mM). Strain RT2T did not grow aerobically.
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DNA of strain RT2T was extracted and the 16S rRNA gene was retrieved as described previously (Abildgaard et al., 2004). Approximately 1900 bp of the dsrAB gene sequence (genes encoding the 
- and 
-subunits of the dissimilatory sulphite reductase) was amplified by PCR from a DNA extract of strain RT2T as well as being cloned as described previously (Mogensen et al., 2005). Plasmid inserts were sequenced as described below using the primers vectorF and vectorR (Thomsen et al., 2001) and a custom-designed internal dsrAB gene sequencing primer (5'-TCGACATCATGAAGGAAGTCG-3') for the sequencing reactions. In addition the apsA gene (encoding the adenosine-5'-phosphosulphate reductase -subunit) was amplified by PCR using the primers APS7-F and APS8-R (Friedrich, 2002), the HotStarTaq system (Qiagen) and thermal cycling according to Friedrich (2002). PCR products of the expected size (900 bp) were cut out of agarose gels, purified and sequenced directly as described below using the primers APS7-F and APS8-R for the sequencing reactions. All PCR products and plasmids were sequenced using an ABI 3100 DNA sequencer (Applied Biosystems) with a DYEnamic ET Terminator sequencing kit (Amersham Biosciences). Sequences of the respective genes were aligned and compiled as described previously (Mogensen et al., 2005). Phylogenetic trees based on 16S rRNA gene sequence datasets were constructed using the distance-matrix, maximum-parsimony and maximum-likelihood algorithms of the ARB program package (Ludwig et al., 2004). A custom-made 50 % conservation filter for 16S rRNA gene sequences from 41 recognized Desulfovibrio species was used to select sequence positions for the analyses. Topologies that could not be resolved unambiguously using the various analyses are shown as multifurcations in the 16S rRNA gene-based phylogenetic consensus tree displayed in Fig. 2, as recommended by Ludwig et al. (1998). To simplify the tree, some species not closely related to strain RT2T were later removed. DsrAB and ApsA amino acid sequence-based phylogenetic trees were inferred using the distance-matrix (FITCH analysis performed according to Friedrich, 2002), maximum-parsimony and maximum-likelihood (with the JTT amino acid replacement model) algorithms for analysis of amino acid sequence data of the ARB program package. Datasets (deduced from dsrAB and apsA gene sequences) including 540 and 241 unambiguously aligned DsrAB and ApsA amino acid sequence positions, respectively, were analysed. Short DsrAB and ApsA amino acid sequences were added to the trees without changing the overall tree topology using the PARSIMONY_INTERAKTIV tool of the ARB program package. Distance matrix-based bootstrap analyses of DsrAB and ApsA amino acid sequence datasets were performed in PAUP* version 4.0b10 (Swofford, 2003). Consensus trees were constructed as described above.
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). A similar affiliation was confirmed by DsrAB and ApsA amino acid sequence analyses (see Supplementary Fig. S2 in IJSEM Online). Pairwise alignment of 16S rRNA gene sequences showed that strain RT2T clearly differs phylogenetically from other Desulfovibrio species. Thus, strain RT2T shared 90.7 and 90.1 % 16S rRNA gene sequence similarity with its closest relatives, Desulfovibrio africanus and Desulfovibrio aminophilus, respectively, over an alignment of 1210 sequence positions. Desulfovibrio africanus is different from strain RT2T in motility (has lophotrichous flagella) and shape (sigmoid instead of vibrio-shaped) and also has a narrower temperature tolerance (Table 1). The pH range of Desulfovibrio africanus is not known and thus cannot be compared. Desulfovibrio aminophilus and strain RT2T are both vibrio-shaped with polar flagella. However, they differ markedly in optimum and cardinal values of pH, temperature and NaCl (Table 1). Furthermore, the range of electron donors utilized by Desulfovibrio aminophilus is larger than that for strain RT2T (Table 1; Baena et al., 1998).
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On the basis of the physiological and molecular properties of strain RT2T and its closest relatives, we propose that strain RT2T should be recognized as representing a novel species of the genus Desulfovibrio. The name Desulfovibrio alkalitolerans sp. nov. is proposed for this organism, in accordance with its ability to grow under alkaline conditions.
Description of Desulfovibrio alkalitolerans sp. nov.
Desulfovibrio alkalitolerans [al.ka.li.to'le.rans. Arabic n. alkali (al-qaliy), the ashes of saltwort; L. pres. part. tolerans tolerating; N.L. part. adj. alkalitolerans alkali-tolerating].
Motile, vibrio-shaped cells with a single polar flagellum and 0.5–0.8x1.4–1.9 µm in size. Non-spore-forming. Alkalitolerant: pH range 6.9–9.9, with optimum growth occurring at 9.0–9.4. NaCl range for growth is 0.085–0.7 % (w/v); optimum growth occurs at 0.13 %. Mesophilic: temperature range for growth is 16–47 °C; optimum growth at 43 °C. Anaerobic, but tolerates short exposure to oxygen. Growth occurs with lactate, pyruvate, formate and hydrogen/acetate as electron donors and sulphate, sulphite and thiosulphate as electron acceptors. Fermentative growth occurs on pyruvate. Yeast extract is required for growth. The genomic G+C content of the type strain is 64.7 mol%.
The type strain, RT2T (=DSM 16529T=JCM 12612T), was isolated from mild steel coupons from a reactor connected to the return line of the Skanderborg district heating plant (Jutland, Denmark).
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ACKNOWLEDGEMENTS |
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