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Faculty of Agriculture, Yamagata University, Wakaba-machi 1-23, Tsuruoka, Yamagata 997-8555, Japan
Correspondence
Atsuko Ueki
uatsuko{at}tds1.tr.yamagata-u.ac.jp
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7, C16 : 15 and C17 : 16. A phylogenetic analysis based on the 16S rRNA gene sequence placed the strain in the class Deltaproteobacteria. The recognized bacterium most closely related to strain MSL86T was [Desulfobacterium] catecholicum DSM 3882T (sequence similarity 94.4 %), and the next most closely related recognized species were Desulfotalea psychrophila (94.2 % sequence similarity with the type strain) and Desulfotalea arctica (93.7 %). As the physiological and chemotaxonomic characteristics of MSL86T were distinctly different from those of any related species, a novel genus and species Desulfopila aestuarii gen. nov., sp. nov. are proposed to accommodate the strain. The type strain of Desulfopila aestuarii is MSL86T (=JCM 14042T=DSM 18488T).
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain MSL86T is AB110542.
Present address: Taisei Corporation, Naze-machi 344-1, Totsuka-ku, Yokohama, Kanagawa 245-0051, Japan. 
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; Kuever et al., 2005). As sulfate levels are sufficient in marine environments, it has been reported that SRBs are responsible for up to 50 % of the organic carbon mineralization in marine sediments (Jørgensen, 1982). Various novel species of SRB have been isolated recently from a wide range of marine sediments (Jeanthon et al., 2002; Sass et al., 2002; Audiffrin et al., 2003; Cravo-Laureau et al., 2004; Moussard et al., 2004; Kuever et al., 2005). In addition, many studies on the diversity of SRB in natural environments have been performed using cultivation-independent molecular techniques based on PCR amplification of the 16S rRNA gene or the dissimilatory sulfite reductase gene (Devereux & Mundfrom, 1994; Voordouw et al., 1996; Wagner et al., 1998; Joulian et al., 2001; Klein et al., 2001; Purdy et al., 2002; Dhillon et al., 2003; Leloup et al., 2006), and these studies have revealed that phylogenetically diverse lineages of uncultivated SRB are still present in natural ecosystems. In the course of an investigation on SRB in an estuarine sediment from a Japanese island, we isolated various sulfite-reducing strains. The phylogenetic, physiological and chemotaxonomic characteristics of one of the strains, MSL86T, supported the proposal of a novel genus and species in the class Deltaproteobacteria. Because strain MSL86T was isolated from estuarine sediment by the dilution colony-counting method using a sample diluted to 10–4, it was thought that the SRB group relating to the strain should be present in the sediment at rather high population levels.
Sediment cores were collected to a depth of 10 cm using a core sampler (5 cm in diameter) from sediment at a water depth of 2 m in the Niida River estuary in Sakata harbour, Japan (i.e. from the Sea of Japan around the Japanese islands; 38° 54.5' N 139° 50.6' E), on 12 November 2000. The sediment sample was subjected to consecutive 10-fold dilutions with seawater bubbled with O2-free N2 gas. The diluted samples (0.2 ml) were inoculated into seawater agar medium (10 ml) containing 20 mM sodium lactate, and viable colony counts for SRB were determined by using the anaerobic roll-tube method (Hungate, 1966). Several strains of SRB were obtained by picking up black colonies of SRB that appeared on the roll-tube agar after incubation for about a month. Strain MSL86T was finally obtained after several purification procedures through colony isolation by the anaerobic roll-tube method.
Two basal media (seawater medium and defined medium) were used in this study. The seawater medium contained the following (l–1 seawater): 0.5 g KH2PO4, 0.3 g NH4Cl, 0.1 g yeast extract, 1 mg sodium resazurin, 10 ml trace element solution (l–1: 10 ml 25 % (v/v) HCl, 1.5 g FeCl2.4H2O, 0.19 g CoCl2.6H2O, 0.1 g MnCl2.4H2O, 0.07 g ZnCl2, 0.062 g H3BO3, 0.036 g Na2MoO4.2H2O, 0.024 g NiCl2.6H2O and 0.017 g CuCl2.2H2O) and 0.5 g L-cysteine hydrochloride monohydrate, as well as an appropriate electron donor. The pH was adjusted to 7.2–7.4 with 1 M NaOH. Agar (Difco) (1.5 %, w/v) was added to the medium and used for the anaerobic roll-tube method for isolation and in slant cultures (with lactate as an electron donor). A medium designated as the ‘defined medium’ (distinguishing it from seawater medium) was used for general physiological characterization of the strain, and contained the following (l–1): 0.5 g KH2PO4, 1.0 g NH4Cl, 1.0 g Na2SO4, 2.0 g MgSO4.7H2O, 0.1 g CaCl2.2H2O, 0.5 g yeast extract, 1 mg sodium resazurin, 10 ml trace element solution, 15 g NaCl and 0.5 g L-cysteine hydrochloride monohydrate (Nakamoto et al., 1996; Ueki et al., 1980; Widdel & Bak, 1992). The pH was adjusted to 7.2–7.4 with 1 M NaOH. Cultivation and transfer of the strain were performed under an O2-free N2 (100 %) atmosphere. The strain was cultivated at 30 °C, unless indicated otherwise. The strain was maintained in slant cultures of the seawater medium or the defined medium with lactate as an electron donor. The pH of both media after autoclaving was around pH 6.3. Each electron donor was added at a final concentration of 20 mM.
The Gram reaction and cellular morphology were confirmed by light microscopy. The motility of the cells was examined by phase-contrast microscopy, and flagella staining was carried out according to Blenden & Goldberg (1965). Growth of the strain under aerobic conditions was examined in the presence of sodium lactate as an electron donor, using the defined medium without L-cysteine and sodium resazurin. The catalase and oxidase activities of the cells were tested as described by Akasaka et al. (2003a). The effects of NaCl concentration and pH on growth of the strain were examined in the presence of sodium lactate as an electron donor, using the defined medium. The effects of temperature on growth were examined using the seawater medium, with sodium lactate as an electron donor. Growth of the strain was monitored by measuring the OD660 with a spectrophotometer (U-1000; Hitachi).
The utilization of electron donors by strain MSL86T was determined by using the defined medium containing each compound at a final concentration of 20 mM. H2 utilization was determined in the presence of acetate (5 mM) and with H2 in the atmosphere. Utilization of electron acceptors was determined with a sulfate-free medium that contained chloride at the same concentration as that of sulfate in the defined medium; sodium lactate (20 mM) served as an electron donor. Sodium sulfite (3 mM), sodium thiosulfate (15 mM) or disodium fumarate (20 mM) was added to the sulfate-free medium as a possible electron acceptor. The utilization of pyruvate, lactate, fumarate or malate (20 mM each) in the absence of electron acceptors in the medium was also determined by using the sulfate-free medium. Fatty acids and amino acids were used in the form of sodium salts and added to the medium from sterilized stock solutions. Utilization of each electron donor or acceptor was determined by comparing growth in the presence and absence of each compound, as well as by measuring the concentration in the medium after cultivation.
Volatile fatty acids and alcohols were analysed by GC (G-5000 or 263-30; Hitachi), as described by Ueki et al. (1986). Non-volatile fatty acids and formate were analysed by HPLC (LC-10AD; Shimadzu), as described by Akasaka et al. (2003a). Sulfate, sulfite and thiosulfate were analysed with an ion chromatograph (Dionex 2000i), as described by Nakamoto et al. (1996). Genomic DNA was extracted according to the method described by Kamagata & Mikami (1991). Extracted DNA was digested with P1 nuclease by using a YAMASA GC kit (Yamasa shoyu) and its G+C content was measured by HPLC with Hitachi L-7400 apparatus equipped with a µBondpack C18 column (3.9x300 mm; Waters). Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and analysed by using a mass spectrometer (JMS-SX102A; JEOL). Whole-cell fatty acids (CFAs) were converted to methyl esters by saponification, methylation and extraction according to the method of Miller (1982). Methyl esters of the CFAs were analysed with a gas chromatograph (Hewlett Packard Hp6890 or Hitachi G-3000) equipped with an HP Ultra2 column. CFAs were identified by means of equivalent chain-lengths (Miyagawa et al., 1979; Ueki & Suto, 1979) according to the protocol of TechnoSuruga, based on the MIDI Microbial Identification System (Microbial ID) of Moore et al. (1994).
The 16S rRNA gene of strain MSL86T was extracted according to the method described by Akasaka et al. (2003a, b) and amplified by PCR using a primer set comprising 27f and 1492r. The PCR-amplified 16S rRNA gene was sequenced by using a Thermo Sequenase primer cycle sequencing kit (Amersham Biosciences) and a DNA sequencer (model 4000L; Li-COR). Multiple alignments of the sequence with reference sequences in GenBank were performed with the BLAST program (Altschul et al., 1997). A phylogenetic tree was constructed with the neighbour-joining method (Saitou & Nei, 1987) by using the CLUSTAL W program (Thompson et al., 1994) as well as the maximum-likelihood program (DNAML) of the PHYLIP 3.66 package (Felsenstein, 2006). All gaps and unidentified base positions in the alignments were excluded before assembly.
The cells of strain MSL86T were Gram-negative rods, 0.7–1.2 µm wide and 1.9–3.8 µm long with rounded ends; they usually occurred singly or in pairs (Fig. 1). The cells were motile by means of single polar flagella. The strain produced thin, greyish colonies on agar slants of the defined medium as well as the seawater medium. Cells of strain MSL86T aggregated during growth in the liquid medium and were deposited at the bottom of the test tubes. Spore formation was not observed.
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Strain MSL86T grew even in the absence of added electron donors, and reduced sulfate with the concomitant production of acetate, suggesting that yeast extract or L-cysteine added to the medium was used as an electron donor. The strain utilized formate, pyruvate, fumarate, ethanol, propanol, butanol and glycerol, as well as lactate, as electron donors for sulfate reduction. Although all organic electron donors were usually oxidized to (mainly) acetate, succinate (2.9 mM) was produced in addition to acetate (8.3 mM) when fumarate was used as the electron donor. Propanol and butanol were oxidized to their corresponding carboxylic acids. Strain MSL86T did not utilize acetate, propionate, butyrate, malate, succinate, methanol, glycine, alanine, serine, aspartate, glutamate or H2 as electron donors.
Strain MSL86T utilized sulfite, thiosulfate and fumarate in addition to sulfate as electron acceptors with lactate as the electron donor. Growth rates in defined medium supplemented with 1.5 % (w/v) NaCl were assessed with fumarate, sulfate, sulfite or thiosulfate as the electron acceptor: the comparison showed that growth was slightly faster with fumarate (µ = 0.096 h–1) than with sulfate (µ = 0.085 h–1), sulfite (µ = 0.052 h–1) and thiosulfate (µ = 0.038 h–1). When fumarate was utilized as an electron acceptor, succinate (3.2 mM) and propionate (1.4 mM) were produced in addition to acetate (7.5 mM), in accordance with the oxidation of lactate (6.7 mM). In the absence of electron acceptors, strain MSL86T oxidized pyruvate (10.4 mM) and produced acetate (7.8 mM) and propionate (2.3 mM). The strain also oxidized fumarate (13.0 mM) without any electron acceptors, and produced acetate (9.5 mM) and succinate (7.0 mM). The strain did not use lactate or malate in the absence of electron acceptors.
The G+C content of the genomic DNA of strain MSL86T was 54.4±0.2 mol%. The major respiratory quinone was MK-8(H4). The predominant CFAs of strain MSL86T were C16 : 0 (33.6 %), C16 : 17 (6.0 %), C16 : 15 (17.1 %) and C17 : 16 (13.7 %). About 66 % of the total CFAs were even-numbered, straight-chain fatty acids. Smaller amounts of hydroxy fatty acids, iso-C11 : 0 3-OH (1.1 %), C14 : 0 3-OH (1.8 %) and C16 : 0 3-OH (1.6 %), and branched C17 : 1 (4.6 %) were also detected.
On the basis of the almost-complete 16S rRNA gene sequence (1471 bp), strain MSL86T is affiliated with the class Deltaproteobacteria. The closest relative (96.3 % sequence similarity) in the public databases was Desulfotalea sp. SFA4, which was isolated from an intertidal flat. The closest known named relative (94.4 % sequence similarity) of strain MSL86T was the SRB [Desulfobacterium] catecholicum DSM 3882T (Szewzyk & Pfennig, 1987). The next most closely related recognized species were Desulfotalea psychrophila (94.2 % similarity to the type strain) and Desulfotalea arctica (93.7 %) of the Desulfobulbaceae (Kuever et al., 2005). Strain MSL86T formed a distinct cluster with strain MSL53, which was isolated from the same sediment as that used to isolate strain MSL86T (Fig. 2); the sequence similarity between these two strains was 98.6 %.
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). The cells of [Desulfobacterium] catecholicum are non-motile and oval to lemon-shaped, whereas strain MSL86T has motile cells that are typically rod-shaped. Furthermore, [Desulfobacterium] catecholicum belongs to the type of SRB that performs complete oxidation (Szewzyk & Pfennig, 1987), whereas strain MSL86T is of the type that performs incomplete oxidation. As other important physiological characteristics of strain MSL86T (including utilization of propionate and butyrate as electron donors for sulfate reduction) also differ from those of [Desulfobacterium] catecholicum (Table 1), strain MSL86T should not be affiliated with the novel genus that is needed to accommodate [Desulfobacterium] catecholicum.
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. Both of the Desulfotalea species (isolated from permanently cold, Arctic, marine sediments) are psychrophilic SRBs and the optimum growth temperatures of Desulfotalea psychrophila and Desulfotalea arctica are 10 and 18 °C, respectively (Knoblauch et al., 1999), whereas strain MSL86T is mesophilic and has an optimum growth temperature of 35 °C. Both of these Desulfotalea species are also SRBs that oxidize incompletely, but the range of electron donors used by strain MSL86T differs from those of these species. Strain MSL86T utilizes glycerol but not malate, whereas Desulfotalea psychrophila utilizes malate but not glycerol. Strain MSL86T utilizes fumarate, propanol and butanol as electron donors, whereas Desulfotalea arctica does not. Strain MSL86T does not use amino acids or H2 (with acetate as a carbon source), unlike both of the Desulfotalea species. The range of electron acceptors used by strain MSL86T is similar to that of Desulfotalea psychrophila but differs from that of Desulfotalea arctica. Desulfotalea arctica does not utilize sulfite or thiosulfate, whereas strain MSL86T utilizes both. In the absence of electron acceptors, strain MSL86T and Desulfotalea psychrophila utilize fumarate, unlike Desulfotalea arctica. Strain MSL86T produced a small amount of propionate, together with acetate, from pyruvate in the absence of electron acceptors. Furthermore, propionate was also produced when fumarate served as an electron acceptor, with lactate as an electron donor. Although some SRBs such as Desulfobulbus and Desulfosarcina species also produce propionate from the fermentation of lactate or pyruvate, these species utilize propionate as an electron donor for sulfate reduction (Kuever et al., 2005). As MSL86T does not utilize propionate as an electron donor, propionate production appears to constitute one of the distinctive physiological characteristics of this strain.
The G+C content of the genomic DNA of strain MSL86T (54.4 mol%) is significantly different from those of Desulfotalea psychrophila (46.8 mol%) and Desulfotalea arctica (41.8 mol%) (Knoblauch et al., 1999). The respiratory quinones of Desulfotalea species are MK-6(H2) or MK-6 (Knoblauch et al., 1999), whereas strain MSL86T possesses MK-8(H4). Many of the SRBs in the class Deltaproteobacteria (including Desulfovibrio species) contain menaquinone MK-6 or MK-6(H2), and some species in the Desulfobacteraceae possess MK-7 or MK-7(H2) (Kuever et al., 2005). Although it is known that Desulfofaba gelida in the Desulfobacteraceae, a psychrophilic SRB, and sulfur-reducing Desulfuromonas species in the Desulfuromonaceae possess MK-8, this is a relatively rare menaquinone in SRBs and related organisms (Kuever et al., 2005). The CFA profiles of strain MSL86T and related Desulfotalea species are compared in Table 2. Even-numbered, unsaturated fatty acids (C16 : 17 and C16 : 15) are the main CFAs found in Desulfotalea species. The high percentages of unsaturated fatty acids (about 90 %) in CFAs of Desulfotalea species probably represent an adaptation to low temperatures (Knoblauch et al., 1999). Strain MSL86T contains much larger amounts of saturated CFAs than do related Desulfotalea species, and the strain contains an odd-numbered, unsaturated fatty acid (C17 : 1) as one of the main CFAs (this being absent, or present as only a minor CFA, in Desulfotalea species). Thus, strain MSL86T has chemotaxonomic characteristics that are distinct from those of the closely related Desulfotalea species.
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Description of Desulfopila gen. nov.
Desulfopila (De.sul.fo.pi'la. L. pref. de from; L. n. sulfur sulfur; L. fem. n. pila pillar; N.L. fem. n. Desulfopila a sulfate-reducing pillar).
Mesophilic. Strictly anaerobic. Cells are Gram-negative, non-spore-forming rods. Sulfate, other inorganic sulfur compounds and fumarate serve as electron acceptors. Organic electron donors are oxidized incompletely to (mainly) acetate. The type species is Desulfopila aestuarii.
Description of Desulfopila aestuarii sp. nov.
Desulfopila aestuarii (ae.stu.a'ri.i. L. gen. n. aestuarii of an estuary).
Has the following characteristics in addition to those described for the genus. Cells are rod-shaped with rounded ends, 0.7–1.2 µm wide and 1.9–3.8 µm long. Motile by a single polar flagellum. Catalase- and oxidase-negative. Colonies are greyish and thin and spread on slant media. The NaCl concentration range for growth is 0–5.0 % (w/v), with an optimum at 1.0 % (w/v). The temperature range for growth is 10–40 °C, with an optimum at 35 °C. Slightly alkaliphilic; the pH range for growth is 6.3–8.5, with optimum growth at pH 7.5–7.6. Utilizes formate, pyruvate, lactate, fumarate, ethanol, propanol, butanol and glycerol as electron donors for sulfate reduction. Does not use acetate, propionate, butyrate, succinate, malate, methanol, glycine, alanine, serine, aspartate, glutamate or H2. Sulfate, sulfite, thiosulfate and fumarate serve as electron acceptors. With fumarate as an electron acceptor and lactate as an electron donor, propionate is produced together with succinate. Pyruvate and fumarate are fermented in the absence of electron acceptors. The genomic DNA G+C content is 54.4 mol%. The major CFAs are C16 : 0, C16 : 17, C16 : 15 and C17 : 16. The major respiratory quinone is MK-8(H4).
The type strain, MSL86T (=JCM 14042T=DSM 18488T), was isolated from an estuarine sediment located in the Sea of Japan around the Japanese islands.
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ACKNOWLEDGEMENTS |
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