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NITE Biological Resource Center, National Institute of Technology and Evaluation (NITE), Kazusakamatari 2-5-8, Kisarazu, Chiba 292-0818, Japan
Correspondence
Tatsunori Nakagawa
nakatats{at}brs.nihon-u.ac.jp
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9c. The G+C content of the genomic DNA was 58.1 mol% for strain FUT3661T and 57.2 mol% for strain Asr22-7T. Phylogenetic analysis based on 16S rRNA gene sequences revealed that the strains were related to members of the genus Ferrimonas (<94.0 % similarities), although the two novel strains formed a separate lineage. 16S rRNA gene sequence similarity between strains FUT3661T and Asr22-7T was 96 %. On the basis of this polyphasic analysis, it was concluded that strains FUT3661T and Asr22-7T represent two novel species within the genus Ferrimonas, for which the names Ferrimonas futtsuensis sp. nov. (type strain FUT3661T=NBRC 101558T=DSM 18154T) and Ferrimonas kyonanensis sp. nov. (type strain Asr22-7T=NBRC 101286T=DSM 18153T) are proposed.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Ferrimonas futtsuensis FUT3661T and Ferrimonas kyonanensis Asr22-7T are AB245515 and AB245514, respectively.
Transmission electron micrographs of cells of strains FUT3661T and Asr22-7T, figures showing the effects of temperature, NaCl concentration and selenate concentration on growth of these two strains and a table detailing their fatty acid contents are available as supplementary material in IJSEM Online.
Present address: Department of Agricultural and Biological Chemistry, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan. 
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, Se(VI)] and selenite [
, Se(IV)] are distributed in oxic environments, while insoluble elemental selenium (Se0) is distributed in anaerobic environments (Conde & Sanz Alaejos, 1997
). The reduction of selenium oxyanions occurs primarily via microbial dissimilatory reduction (Stolz & Oremland, 1999). Moreover, the microbial reduction of soluble Se(VI) to insoluble Se0 is an important process in the removal of Se(VI) from Se-contaminated water. In recent years, several bacteria capable of reducing selenate to elemental selenium have been isolated from different environments. These isolates include Bacillus sp. SF-1 from a selenium-polluted sediment (Fujita et al., 1997), Bacillus selenitireducens MLS10T from alkaline lake sediments (Switzer Blum et al., 1998), Sulfurospirillum barnesii SES-3T from freshwater sediments (Stolz et al., 1999), Selenihalanaerobacter shriftii DSSe-1T from deep-sea sediments (Switzer Blum et al., 2001), Salana multivorans Se-3111T from an aerobic bioreactor (von Wintzingerode et al., 2001) and Citrobacter freundii Iso-Z7 from selenium-contaminated sediment (Zhang et al., 2004). Recently, a dissimilatory metal-ion-reducing bacterium, Shewanella oneidensis MR-1T, within the Gammaproteobacteria was found to reduce selenite to elemental selenium (Klonowska et al., 2005). Here we report the characterization of novel mesophilic, facultatively anaerobic bacteria belonging to the Gammaproteobacteria, which are related to the genus Ferrimonas and are able to reduce selenate to elemental selenium. Given that the type strain of the type species of the genus Ferrimonas, Ferrimonas balearica PATT, is known to be an iron(III)- and manganese(IV)-reducing bacterium (Rosselló-Mora et al., 1995), the reduction of selenate, selenite, iron(III) and manganese(IV) was investigated in the novel isolates and in the type strains of recognized members of the genus Ferrimonas.
Sediment samples were collected with an Eckman grabber from a mudflat at Futtsu beach on the coast of Tokyo Bay, Japan. Black-coloured sediments were recovered from cores by means of plastic syringes, immediately put into 150 ml sterilized serum bottles containing 100 ml modified bicarbonate-buffered (MBB) medium without electron donor and acceptor and then sealed with a butyl rubber cap under a gas phase of 100 % N2. The samples were transferred to our laboratory within a few hours. A sample of the slurry (1 ml) was used to inoculate 30 ml MBB medium that was prepared anaerobically under N2/CO2 (80 : 20, v/v; Widdel & Bak, 1992), the gas mixture being supplied through a deoxygenized gas pressure injector (IP-8; Sanshin Industrial). The basal medium was composed of 20 g NaCl l–1, 3 g MgCl2.6H2O l–1, 0.15 g CaCl2.2H2O l–1, 0.25 g NH4Cl l–1, 0.2 g KH2PO4 l–1 and 0.5 g KCl l–1. The following were added per litre of the basal medium: 1 ml non-chelated trace element mixture (Widdel et al., 1983), 1 ml selenite/tungstate solution (0.4 g NaOH l–1, 6 mg Na2SeO3.5H2O l–1, 8 mg Na2WO4.2H2O l–1), 30 ml bicarbonate solution (84 g NaHCO3 l–1), 1 ml vitamin mixture [40 mg 4-aminobenzoic acid l–1, 10 mg D-biotin, 100 mg nicotinic acid l–1, 50 mg calcium D-pantothenate l–1 and 150 mg pyridoxine dihydrochloride l–1 dissolved in 10 mM sodium phosphate buffer (pH 7.1)], 1 ml thiamine solution [100 mg thiamine chloride dihydrochloride l–1 dissolved in 25 mM sodium phosphate buffer (pH 3.4)] and 1 ml vitamin B12 solution (50 mg cyanocobalamine l–1 dissolved in distilled water). The pH of the medium was adjusted with 1 M HCl or 1 M CaCO3 to 7.0. Selenate (1 M) and lactate (2 M) were separately autoclaved and added to the medium to a final concentration of 5 mM as an electron acceptor and electron donor, respectively. Serum bottles (70 ml) sealed with butyl rubber stoppers under a headspace of N2/CO2 (80 : 20, v/v) were used for cultivation. The inoculated cultures were incubated at 25 °C in the dark and shaken by hand for a few seconds every week. An orange- to red-coloured precipitate formed in the culture as a result of the formation of insoluble elemental selenium. Several elemental selenium-forming enrichment cultures were established by subculturing twice in the same medium. The enrichment cultures were diluted in anaerobic molten agar (1.1 %, w/v; Bacto) of the same medium, and orange- to red-coloured colonies were obtained in the agar shake tubes. Purification of the colonies by the agar shake tube method was repeated twice before aerobic plating on a marine agar 2216 (MA; Difco) plate. A single colony on the MA plate was incubated back into MBB medium containing 5 mM selenate and 5 mM lactate and, after several days, red-coloured precipitate developed in the culture due to the formation of insoluble elemental selenium. This isolate was designated strain FUT3661T. The purity of the final culture was confirmed by microscopic examination and partial sequencing of the 16S rRNA gene using appropriate PCR primers.
Littleneck clams, Ruditapes philippinarum, were collected at Kyonan beach on the coast of Tokyo Bay and maintained in an atmosphere of 100 % CO2 during transfer to our laboratory. The clams were dissected, and approximately 1 g alimentary tract homogenate was used for the isolation of bacteria. Serial decimal dilutions (10–1–10–10) of the alimentary tract extracts were made with saline; 0.1 ml dilutions were spread on LYPm agar plates and cultivated at room temperature (approximately 23 °C) in an atmosphere that contained 100 % CO2 for 1 month or more. LYPm medium was composed of 10 g 
-lactose, 10 g yeast extract (Difco), 5 g polypeptone (Nihon Seiyaku), 20 g NaCl, 0.025 g Tween 80, 5 ml of salt solution and 1 ml distilled water; the initial pH of the medium was adjusted to 6.0. The salt solution contained (per litre of distilled water) 40 mg MgSO4.7H2O, 2 mg MnSO4.4H2O, 2 mg FeSO4.7H2O and 2 mg NaCl. Visible colonies grown on LYPm agar medium were collected and the purification procedure was repeated several times until the cultures were deemed to be pure. The first pure culture was designated strain Asr22-7T. The purity of the final culture was confirmed by microscopic examination and partial sequencing of the 16S rRNA gene using appropriate PCR primers. Strain Asr22-7T was maintained on MA plates. Several experiments for selenate reduction by strain Asr22-7T were performed anaerobically with MBB medium. An orange-coloured precipitate developed in the culture bottle during incubation at 25 °C as a result of the formation of insoluble elemental selenium.
Cells were observed under a phase-contrast microscope (AX70; Olympus). Gram staining was carried out using a standard procedure (Hucker & Conn, 1923) with Enterococcus faecalis NBRC 100481T as a positive control for the staining. Cells of strain FUT3661T grown to late-exponential phase at 30 °C in marine broth 2216 (MB, pH 7.0; Difco) supplemented with NaCl to 3.0 % (w/v), and those of strain Asr22-7T grown to the same growth phase in MB at 25 °C, were negatively stained with 1 % (w/v) phosphotungstic acid and observed under a Hitachi transmission electron microscope at an accelerating voltage of 80 kV. Cells of strain FUT3661T were Gram-negative, motile rods (0.7–0.9x0.4–0.7 µm), as were those of strain Asr22-7T (0.7–1.1x0.5–0.8 µm). Cells of both strains possessed a polar monotrichous flagellum (see Supplementary Fig. S1 in IJSEM Online). In most cases, strains FUT3661T and Asr22-7T appeared as single cells. No endospore production was observed.
Strains FUT3661T and Asr22-7T grew rapidly both in MB and on MA under aerobic conditions. The doubling time of strain FUT3661T incubated aerobically in MB (pH 7.0; NaCl 3.0 %) at 30 °C was 48 min, whereas that of strain Asr22-7T incubated aerobically in MB (pH 7.0; NaCl 2.0 %) at 25 °C was 78 min. To determine the optimum growth temperature and NaCl concentration under selenate-reducing conditions, tubes with MBB medium containing 5 mM selenate and 5 mM lactate were inoculated with the two novel strains and cultivated anaerobically without shaking in the dark for 2 weeks (Table 1). Growth of the strains was determined according to the optical density of the tubes at 600 nm. All experiments were conducted in duplicate. Strain FUT3661T grew at temperatures between 15.0 and 30.0 °C, with optimal growth at 30.0 °C (see Supplementary Fig. S2 in IJSEM Online). Strains FUT3661T and Asr22-7T required NaCl for growth (see Supplementary Fig. S3 in IJSEM Online). The ability to grow at pH 5.5–9.0 was tested in MBB medium containing 5 mM selenate and 5 mM lactate.
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). All potential electron acceptors, e.g. 5 mM selenate (Na2SeO4), 5 mM selenite (Na2SeO3), 0.01 g iron(III) oxyhydroxide [Fe(OH)3] ml–1 (Lovley & Phillips, 1986), 5 mM iron(III) citrate (FeC6H5O7), 5 mM arsenate (Na2HAsO4), 0.03 g manganese(IV) oxide (MnO2) ml–1, 0.01 g elemental sulfur (S0) ml–1, 5 mM thiosulfate (Na2S2O3), 5 mM sulfate (Na2SO4), 5 mM nitrate (NaNO3) and 20 % (in the head space) oxygen (O2), were tested in MBB medium supplemented with 5 mM lactate. All experiments were conducted in duplicate. The concentrations of selenate, arsenate and nitrate in the cultivated tube were analysed via HPLC (2695; Waters). The amounts of total arsenic [As(V) and As(III)], reduced manganese and nitrite in the cultures were analysed with Pack Test kits (WAK-As, -Mn and -NO2; Kyoritsu Chemical-Check Lab). The amount of iron(II) in the cultures was measured with the phenanthroline method (Tamura et al., 1974). Hydrogen sulfides produced from elemental sulfur, thiosulfate and sulfate in the incubated media were measured with the methylene blue formation reaction method (Cline, 1969). The production of nitrite from nitrate was also tested via the API 20 NE system (bioMérieux). Cell density in the cultures was determined by counting cells using epifluorescence microscopy after filtration of paraformaldehyde-fixed cells stained with 4',6-diamidino-2-phenylindole (DAPI) through polycarbonate Nucleopore (Millipore) membranes (0.2 µm pore size) (Porter & Feig, 1980). Strain FUT3661T was able to utilize selenate, iron(III) oxyhydroxide, iron(III) citrate, arsenate, manganese(IV) oxide, elemental sulfur, thiosulfate, nitrate and oxygen (Table 1), the yield with each electron acceptor being 6x107, 1x108, 6x107, 6x107, 6x107, 1x108, 2x108, 6x107 and 6x107 cells ml–1, respectively. Nitrate was reduced to nitrite. No growth of strain FUT3661T was observed in the culture with selenite (1x106 cells ml–1). Strain Asr22-7T was able to utilize selenate, iron(III) oxyhydroxide, iron(III) citrate, arsenate, manganese(IV) oxide, elemental sulfur, nitrate and oxygen (Table 1), the yield with each electron acceptor being 6x107, 6x107, 1x108, 9x107, 5x107, 1x108, 8x107 and 2x108 cells ml–1, respectively. Nitrate was reduced to nitrite. No growth of strain Asr22-7T was observed in the culture with selenite.
The optimal selenate concentration for growth in test tubes containing MBB medium supplemented with several concentrations of selenate and 5 mM lactate was determined at 30 °C for strain FUT3661T and at 25 °C for strain Asr22-7T without shaking in the dark for 2 weeks. Growth was assessed based on the optical density of the tubes at 600 nm. All experiments were conducted in duplicate. The optimal selenate concentrations for growth of strains FUT3661T and Asr22-7T were 12.5 and 5.0 mM, respectively (see Supplementary Fig. S4 in IJSEM Online). The time courses of the reduction of selenate and concomitant bacterial growth of strains FUT3661T and Asr22-7T were examined in 150 ml serum bottles containing 120 ml of anaerobic MBB medium supplemented with 12.5 mM selenate, 10 mM lactate and 0.01 % (w/v) yeast extract for strain FUT3661T, and 5 mM selenate, 5 mM lactate and 0.01 % (w/v) yeast extract for strain Asr22-7T (Fig. 1). Cultures were sampled periodically and analysed for cell density by staining paraformaldehyde-fixed cells with DAPI. The experiments were conducted in triplicate. The concentrations of selenate decreased, accompanied by precipitation of elemental selenium, during growth of the two strains. Thus, strains FUT3661T and Asr22-7T were found to be facultatively anaerobic, selenate-reducing chemo-organotrophs.
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Strains FUT3661T and Asr22-7T produced H2S on triple-sugar iron (TSI) plates (Difco), and hydrolysed gelatin (API 20 NE system; bioMérieux). Strain Asr22-7Tshowed a positive reaction for arginine dehydrolase on the same API system.
For quinone analyses, strain FUT3661T was grown in MB containing 3 % (w/v) NaCl at pH 7.0 at 30 °C, while strain Asr22-7T was grown in MB at pH 7.0 at 25 °C. Isoprenoid quinones were extracted from freeze-dried cells with chloroform/methanol (2 : 1, v/v) and fractionated by TLC (Collins et al., 1977). Menaquinone and ubiquinone for the LC-MS (LCMS-8000, Shimadzu) analysis were excised from the chromatographs. The LC-MS analysis indicated that strains FUT3661T and Asr22-7T contained menaquinones (MK-7) and ubiquinones (Q-7 and Q-8) as the predominant isoprenoid quinones. Similarly, strains of the genus Ferrimonas also contained MK-7, Q-7 and Q-8 (Katsuta et al., 2005). The major cellular fatty acid contents of strains FUT3661T and Asr22-7T were analysed by GC (Agilent GC 6890N; MIDI Inc.). The two novel strains were grown to late-exponential growth phase in MB containing 3 % NaCl at pH 7.0 at 30 °C, and in MB at pH 7.0 at 25 °C and the cellular fatty acids were extracted from the cells and converted to methyl esters according to the manufacturer's recommendations. The major cellular fatty acids of strains FUT3661T and Asr22-7T were C16 : 19c and C16 : 0 (see Supplementary Table S1 in IJSEM Online), contrasting with the results for members of the genus Ferrimonas grown in MB (Katsuta et al., 2005) (Table 1).
Genomic DNA was extracted from cells grown in MB. The G+C content of the DNA of strains FUT3661T and Asr22-7T was 58.1 and 57.2 mol%, respectively, as determined by direct analysis of the deoxyribonucleosides using HPLC (Tamaoka & Komagata, 1984; Mesbah et al., 1989). The 16S rRNA gene was amplified by PCR using Eubac27F and 1492R primers (DeLong, 1992). The sequence of the PCR product was directly determined in both strands by the dideoxynucleotide chain-termination method with a BigDye v3.1 sequencing kit (PE Applied Biosystems) and a DNA sequencer (model 3100; PE Applied Biosystems) according to the manufacturers' recommendations. We searched for sequences similar to the 16S rRNA gene sequences of these strains in the databases of the National Center for Biotechnology Information and DNA Database of Japan using the BLAST (Altschul et al., 1997) and FASTA programs (Lipman & Pearson, 1985). The 16S rRNA gene sequences of strains FUT3661T and Asr22-7T were most closely related to the sequence of a marine, facultative iron(III)-reducing bacterium, F. balearica PATT, isolated from the surface sediment of a harbour (Rosselló-Mora et al., 1995) with 93.8 and 93.7 % similarity, respectively. Phylogenetic analysis was performed using MEGA3 software (Kumar et al., 2004). The Kimura two-parameter model was used to estimate pairwise distances. Phylogenetic trees were inferred by the neighbour-joining and maximum-parsimony methods. Bootstrap values were determined from 1000 replications. The phylogenetic tree constructed from the data indicated that strains FUT3661T and Asr22-7T clustered within the Gammaproteobacteria encompassing the genus Ferrimonas, including F. balearica PATT (Rosselló-Mora et al., 1995) and F. marina A4D-4T (Katsuta et al., 2005), but represented a novel lineage (Fig. 2). DNA–DNA hybridization experiments were performed using the fluorometric microdilution plate method (Ezaki et al., 1988) to determine the genetic relatedness between strains FUT3661T and Asr22-7T, and between the two novel strains and F. balearica PATT and F. marina A4D-4T. Strains FUT3661T and Asr22-7T showed a mean DNA–DNA relatedness of 2.9 % when their DNAs were used individually as labelled DNA probes for cross-hybridization. These data demonstrate that strains FUT3661T and Asr22-7T represent members of different genomic species. Strain FUT3661T showed mean DNA–DNA relatedness of 0.4 % to F. balearica PATT and 0.2 % to F. marina A4D-4T. Strain Asr22-7T showed mean DNA–DNA relatedness of 5.9 % to F. balearica PATT and 9.2 % to F. marina A4D-4T.
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and Fig. 1). Moreover, strains FUT3661T and Asr22-7T can each be considered to represent a different species based on DNA–DNA hybridization analysis together with differences in DNA G+C content and in their phenotypic properties (Table 1 and Fig. 2; see also Supplementary Figs S2, S3 and S4 in IJSEM Online). We propose the names Ferrimonas futtsuensis sp. nov. and Ferrimonas kyonanensis sp. nov. to accommodate these two novel strains.
Description of Ferrimonas futtsuensis sp. nov.
Ferrimonas futtsuensis (fut.tsu.en'sis. N.L. fem. adj. futtsuensis from Futtsu, the place of isolation).
Cells are Gram-negative rods (0.7–0.9x0.4–0.7 µm) and motile by a polar flagellum. No spores are observed. Mesophilic, facultatively anaerobic, chemo-organotroph. Circular, opaque, beige colonies are formed after 2 days on MA plates at 30 °C. Growth occurs at 15.0–30.0 °C, with an optimum at 30.0 °C. The pH range for growth is 6.0–9.0. NaCl is required for growth; growth occurs at 0.7–5.0 % (w/v), with an optimum at 3.0 %. Major isoprenoid quinones are MK-7, Q-7 and Q-8. Major cellular fatty acids are C16 : 0 (19.4 %), C16 : 19c (20.4 %) and C18 : 19c (15.9 %). Growth is observed with yeast extract, tryptone, Casamino acids, pyruvate, fumarate, propionate and lactate as the electron donor and carbon source in the presence of selenate. Gelatin is hydrolysed. Utilizes selenate, iron(III) oxyhydroxide, iron(III) citrate, arsenate, manganese(IV) oxide, elemental sulfur, thiosulfate and oxygen as an electron acceptor. Can reduce selenate to elemental selenium. The G+C content of the genomic DNA is 58.1 mol% (as determined by HPLC).
The type strain, FUT3661T (=NBRC 101558T=DSM 18154T), was isolated from Futtsu beach on the coast of Tokyo Bay, Japan.
Description of Ferrimonas kyonanensis sp. nov.
Ferrimonas kyonanensis (ky.o.nan.en'sis. N.L. fem. adj. kyonanensis from Kyonan, the place of isolation).
Cells are Gram-negative rods (0.7–1.1x0.5–0.8 µm) and motile by a polar flagellum. No spores are observed. Mesophilic, facultatively anaerobic, chemo-organotroph. Circular, opaque, beige colonies are formed after 2 days on MA at 25 °C. Growth occurs at 15.0–32.5 °C, with an optimum at 25.0–28.0 °C. The pH range for growth is 6.0–9.0. NaCl is required for growth; growth occurs at 2.0–5.0 % (w/v), with an optimum at 2.0 %. Major isoprenoid quinones are MK-7, Q-7 and Q-8. Major cellular fatty acids are C16 : 0 (15.6 %), C16 : 19c (28.5 %) and C18 : 19c (10.9 %). Growth is observed with yeast extract, tryptone, Casamino acids, pyruvate and lactate as the electron donor and carbon source in the presence of selenate. Gelatin and arginine are hydrolysed. Utilizes selenate, iron(III) oxyhydroxide, iron(III) citrate, arsenate, manganese(IV) oxide, elemental sulfur, nitrate and oxygen as an electron acceptor. Reduces selenate to elemental selenium. The G+C content of the genomic DNA is 57.2 mol% (as determined by HPLC).
The type strain, Asr22-7T (=NBRC 101286T=DSM 18153T), was isolated from the alimentary tract of littleneck clams collected from Kyonan beach on the coast of Tokyo Bay, Japan.
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ACKNOWLEDGEMENTS |
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, MnO2 and S0 were utilized by strains 1–4. Fe(III) citrate, O2 and lactate were utilized by all strains. NO3– was utilized by strains 1–3. 
was not utilized by strains 1–4.
