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1 Faculty of Agriculture, Yamagata University, Wakaba-machi 1-23, Tsuruoka 997-8555, Japan
2 Laboratory of Applied Microbiology, Marine Biotechnology Institute, Heita 3-75-1, Kamaishi 026-0001, Japan
Correspondence
Atsuko Ueki
uatsuko{at}tds1.tr.yamagata-u.ac.jp
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains SV434T and S562 are AB264625 and AB264624, respectively. The accession numbers of the 16S rRNA gene sequences of the other five isolates are AB264621, AB264623, AB264626, AB264628 and AB264629.
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) seem to predominate, as they have been detected in many different reactors irrespective of the types of waste being treated (Chouari et al., 2005; Godon et al., 1997; Levén et al., 2007). In the case of the phylum Bacteroidetes, species belonging to the Bacteroides–Prevotella group are major constituents, mainly comprising micro-organisms derived from human faecal and oral sources as well as others from mammalian organs such as the rumen (Holdeman et al., 1984; Paster et al., 1994). Bacterial clones affiliated with the group are often detected as dominant components of the microflora in methanogenic reactors (Chouari et al., 2005; Godon et al., 1997; Levén et al., 2007), but few bacterial strains affiliated with the group have ever been isolated from such environments. Thus, the exact properties of bacteria related to the Bacteroides–Prevotella group detected in methanogenic reactors by molecular techniques remain to be clarified. In this study, phylogenetic, physiological, ecological and chemotaxonomic characteristics of two strains (SV434T and S562) isolated from a rice-straw residue sample from a methanogenic reactor treating waste from cattle farms were determined. The strains were found to be strictly anaerobic, slightly alkaliphilic, Gram-negative rods requiring haemin and cobalamin for growth and producing acetate and propionate from glucose.
Strains SV434T and S562 were isolated from a rice-straw residue sample obtained from a methanogenic reactor used to treat waste collected from cattle farms (comprising up to 1000 cattle in total) in Betsukai-machi in Hokkaido, Japan. The reactor was a vertical cylindrical type (1500 m3) operated at 35 °C. The waste treated in the reactors consisted of rice straw (which is used as matting in the cattle farms) together with the faeces and urine of the animals. Both strains were isolated by using the anaerobic roll-tube method for enumeration of anaerobic fermentative bacteria by the colony-counting method (Hungate, 1966; Holdeman et al., 1977), using PY4S agar (see below) in the presence or absence of the B-vitamin mixture (see below). Anaerobic sludge samples obtained from the reactor were filtered through a mesh (2 mm pore size) and the relatively large residue of rice straw that remained on the mesh was collected. The rice-straw samples obtained were washed several times with sterile anoxic diluent and homogenized in a Waring blender (10 000 r.p.m. for 10 min) under N2 gas (Kaku et al., 2000; Akasaka et al., 2003a). The homogenized samples were successively diluted anaerobically and used as inocula for the anaerobic roll-tube agar in the isolation of anaerobic fermentative bacteria (Akasaka et al., 2003a, 2004). Colonies that formed on the agar during incubation for 2 weeks were picked at random and about 50 isolates were obtained from a sample. Two strains (SV434T and S562) were selected (out of seven strains) as representatives of the isolates and were found to be closely related to each other according to 16S rRNA gene sequence data and showed similar phenotypic properties. Strain SV434T was picked from anaerobic roll-tube agar inoculated with a 10–4-diluted sample using PY4S agar containing a B-vitamin mixture (see below) and strain S562 was isolated from a 10–5-diluted sample with PY4S agar.
The strains were cultivated anaerobically at 30 °C (unless otherwise indicated) using peptone/yeast extract (PY) medium as the basal medium with oxygen-free mixed gas (N2/CO2, 95 : 5) as the headspace, as described by Ueki et al. (2006a). PY medium supplemented (l–1) with 0.25 g each of glucose, cellobiose, maltose and soluble starch as well as 15 g agar (Difco) was designated PY4S agar and used for maintenance of the strains in agar slants. PY liquid medium supplemented with haemin (at a final concentration of 5 mg l–1) (Holdeman et al., 1977) (PYH medium) and a B-vitamin mixture (10 ml l–1) (PYHV medium) as well as 10 g glucose l–1 (PYHVG medium) was used for cultivation of the strains for various physiological tests and chemotaxonomic analyses of the cells unless otherwise indicated (Ueki et al., 2006b). Since both strains were slightly alkaliphilic (as described below), the pH of these liquid media was adjusted to pH 7.6–7.7 using bicine [N,N-bis(2-hydroxyethyl)glycine] (Good's buffer; Dotite) (20 mM). For the medium, KH2PO4 was replaced with K2HPO4 and Na2CO3 was omitted from the PY basal medium by using an atmosphere comprising 100 % N2. The composition of the B-vitamin mixture used was as follows (100 ml–1): 0.1 mg biotin, 0.1 mg cyanocobalamin (vitamin B12), 0.3 mg p-aminobenzoic acid, 0.5 mg folic acid, 0.5 mg thiamine hydrochloride, 0.5 mg riboflavin and 1.5 mg pyridoxine hydrochloride (Akasaka et al., 2004). Growth in liquid medium was monitored using changes in the OD660.
Growth of the strains under aerobic conditions was examined as described previously (Ueki et al., 2006a). Spore formation was assessed by observing cells after Gram-staining. Oxidase and nitrate-reducing activities were determined according to methods described by Akasaka et al. (2003b). Catalase activity was examined using cells cultivated in liquid media and collected by centrifugation. A small amount of H2O2 solution (3 %, v/v) was mixed with the cell pellet and the production of bubbles of O2 checked. Catalase activity was also examined using H2O2 solution: this was added to slant cultures of PY4S agar both before and after they had been exposed to air for more than 30 min (Wilkins et al., 1978). Utilization of carbon sources was tested in PYHV liquid medium (pH 7.6–7.7), each substrate being added at 10 g l–1 (for sugars and sugar alcohols) or 30 mM (organic acids). Utilization of each substrate was determined from growth measurements (OD660) as well as by determining changes in the pH of the medium after cultivation. Bile sensitivity was determined using the addition of bile salts (Oxoid) (0.1–0.5 %, w/v) to PYHVG medium. Fermentation products were analysed by GC or HPLC as described previously (Ueki et al., 1986; Akasaka et al., 2003a). Other characterizations were performed according to the methods described by Holdeman et al. (1977) and Ueki et al. (2006a, b).
Cellular fatty acids (CFAs) were converted to methyl esters according to the method of Miller (1982) and analysed by GC (HP6890 from Hewlett Packard or G-3000 from Hitachi) equipped with an HP Ultra 2 column. CFAs were identified from equivalent chain lengths (Miyagawa et al., 1979; Ueki & Suto, 1979) according to the protocol of TechnoSuruga (Moore et al., 1994). Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and analysed by using a mass spectrometer (JMS-SX102A; JEOL). Genomic DNA, extracted according to the method described by Akasaka et al. (2003b), was digested with P1 nuclease by using a YAMASA GC kit (Yamasa shoyu) and its G+C content was measured by HPLC apparatus (L-7400; Hitachi) equipped with a µBondapack C18 column (3.9x300 mm; Waters).
PCR amplification of the V3 region of the 16S rRNA gene for denaturing gradient gel electrophoresis was performed, using 341f with a GC clamp and 534r as the primer set (Muyzer et al., 1993), with DNA extracted as described previously (Akasaka et al., 2003b). The denaturing gradient gel electrophoresis was carried out with 10 % (v/v) polyacrylamide gels with a urea/formamide gradient (30–60 %), by using a DCode system (Bio-Rad). A 100 % denaturing solution was defined as 7 M urea plus 40 % formamide. The gels were run at 200 V for 4 h at 58 °C and stained with SYBR Gold (Invitrogen). An almost-complete 16S rRNA gene was PCR amplified using primers 27f and 1492r or 8f and 1546r. The PCR-amplified 16S rRNA gene was sequenced by using a Thermo Sequenase primer cycle sequencing kit (Amersham Biosciences) and a DNA sequencer (4000L; LI-COR) or an ABI Prism BigDye Terminator cycle sequencing ready reaction kit and an ABI Prism 3730 automatic DNA sequencer (Applied Biosystems). Multiple alignments of the sequences 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). All gaps and unidentified base positions in the alignments were excluded before sequence assembly.
Strains SV434T and S562 had almost the same properties. Of the characteristics described below, detailed data such as growth rates and amounts of end products given here are based mainly on the data for strain SV434T (as a representative strain).
Cells of the strains were Gram-negative rods, 0.7–0.8 µm wide and 1.3–2.1 µm long; some longer (4–12 µm) cells also occurred (Fig. 1a, b). Extraordinarily long rods sometimes occurred, depending on the culture (Fig. 1c). Cells were non-motile, as observed using phase-contrast microscopy. Both strains grew very thinly as translucent colonies with smooth surfaces on PY4S agar. The strains could not grow in air, on either PY4S agar or nutrient agar. Spore formation was not observed.
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Catalase activity was not detected in cells grown in PY4S agar slants or in PYG liquid medium, but cells grown in the presence of haemin (PYHG or PYHVG medium) usually possessed this enzyme activity. Oxidase activity was not detected. Both strains utilized arabinose, fructose, galactose, glucose, mannose, cellobiose, maltose, glycogen, soluble starch, dextrin, amygdalin, lactate and pyruvate as growth substrates. Lactose, aesculin, and fumarate were utilized only weakly. Acids were produced from all of these substrates. The strains did not use ribose, xylose, rhamnose, sorbose, melibiose, sucrose, trehalose, melezitose, raffinose, CM-cellulose, cellulose powder, filter paper, xylan, pectin, inulin, salicin, glycerol, dulcitol, inositol, mannitol, sorbitol, ethanol, malate or succinate.
Acetate (2.7 mM), propionate (1.9 mM), lactate (13.9 mM) and a trace amount of succinate (0.4 mM) were produced as fermentation products in PYG medium after 2 weeks cultivation, while acetate (9.7 mM) and propionate (15.4 mM) and a trace amount of succinate (0.4 mM) were produced in the presence of haemin and vitamin (PYHVG medium) after 48 h cultivation. Acetate (10.2 and 16.8 mM) and propionate (20.9 and 12.8 mM) were produced from lactate and pyruvate, respectively. Aesculin was hydrolysed, but gelatin was not. Urease, hydrogen sulfide and indole were not produced. The strains did not reduce nitrate and could not grow in the presence of 0.1 % (w/v) bile salts.
The pH for optimum growth was about 7.9 and both strains failed to grow at initial pH values lower than 5.7 and higher than 8.9. Growth rates (µ) at pH 7.9 and 6.6 were 0.41–0.45 and 0.21 h–1, respectively. The final pH after growth in PYHVG medium (initial pH 7.6) was about pH 5.1. The temperature range for growth was 5–35 °C, the optimum being 30 °C (µ=0.38 h–1 at pH 7.6). Both strains grew at 35 °C but not at 37 °C. The growth rate at 10 °C was relatively high (µ=0.064 h–1). The NaCl concentration range for growth was rather broad (0–4.0 %, w/v) and optimum growth occurred at 1.0 % (w/v) NaCl in PYHVG medium.
The major CFAs of strain SV434T were anteiso-C15 : 0 (41.2 %), iso-C17 : 0 (16.1 %), anteiso-C17 : 0 (14.0 %) and iso-C15 : 0 (6.3 %), with smaller amounts of C15 : 0 (2.8 %), C16 : 0 (2.5 %), iso-C16 : 0 (2.3 %), iso-C12 : 0 (1.9 %), anteiso-C13 : 0 (1.7 %) and C17 : 0 (1.6 %). Strain S562 had a somewhat different profile: anteiso-C15 : 0 (42.8 %), iso-C15 : 0 (9.9 %) and iso-C17 : 0 3-OH (8.8 %) were the major CFAs, smaller proportions of C14 : 0 (2.0 %), C15 : 0 (4.0 %), C16 : 0 (1.9 %), iso-C17 : 0 (2.8 %) and anteiso-C17 : 0 (2.2 %) were also present and various hydroxy fatty acids such as C15 : 0 3-OH (3.8 %), iso-C15 : 0 3-OH (4.7 %), anteiso-C15 : 0 3-OH (1.2 %), C16 : 0 3-OH (4.3 %) and anteiso-C17 : 0 3-OH (3.0 %) were found. The G+C contents of the genomic DNAs were 46.2 mol% (strain SV434T) and 47.5 mol% (strain S562). The menaquinones MK-8(H0) and MK-9(H0) were the predominant respiratory quinones in both strains. Trace amounts of menaquinone MK-10(H0) may also be present.
Denaturing gradient gel electrophoresis analysis of the V3 region of the 16S rRNA gene in strains SV434T and strain S562 produced the same banding pattern, with two clearly separated bands (separated by more than 7 mm under the conditions described above), indicating that both strains had at least two different copies of the 16S rRNA gene. 16S rRNA gene sequences were determined for both strains (1428 bp for strain SV434T and 1387 bp for strain S562): they had the same sequence. The nucleotide at position 467 (corresponding to the numbering of Escherichia coli sequence) was determined as Y, i.e. C or T, and the presence of two different sequences in the V3 region of the 16S rRNA gene was confirmed.
Both strains were assigned to the phylum Bacteroidetes (Garrity & Holt, 2001) on the basis of the 16S rRNA gene sequences determined. For both strains, the most closely related type strain was Bacteroides coprosuis CCUG 50528T (Whitehead et al., 2005), with a sequence similarity of 95.9 % based on the sequence of strain SV434T (the aforementioned Y was replaced with T for the similarity calculations). The next most closely related type strains were those of Bacteroides intestinalis (Bakir et al., 2006) (sequence similarity, 93.5 %) and Bacteroides thetaiotaomicron (93.2 %) (Holdeman et al., 1984). Strains SV434T and S562 formed a branch that was separate from those of closely related Bacteroides species in the phylogenetic tree composed of related Bacteroides species (Fig. 2).
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; Paster et al., 1994). Of the Bacteroides species with validly published names, B. coprosuis (Whitehead et al., 2005) and some cellulolytic or xylanolytic species including Bacteroides cellulosolvens (Murray et al., 1984) and Bacteroides xylanolyticus (Scholten-Koerselman et al., 1986) were derived from pig manure or sewage sludge. The latter two species, however, have been recognized as belonging to the phylum Firmicutes, on the basis of 16S rRNA gene sequences (Schwarz, 2001; GenBank accession numbers L35517 and DQ497992, respectively). Thus, to our knowledge, B. coprosuis (isolated from swine-manure storage pits and described recently by Whitehead et al., 2005) may be the only recognized Bacteroides species to have been derived from habitats other than animals.
Strains SV434T and S562 have characteristics that differ significantly from those of their closest relatives (Table 1). The optimum growth temperature for strains SV434T and S562 is 30 °C, whereas the three recognized Bacteroides species have an optimum temperature of 37 °C. The DNA G+C contents of strains SV434T and S562 are in the range 46–47 mol%, whereas that of B. coprosuis CCUG 50528T is 36.4 mol%, although the values for our novel strains are similar to those of the other two related species and to those of other Bacteroides species (Holdeman et al., 1984; Shah & Collins, 1983). The predominant respiratory quinones (MK-8 and MK-9) in the novel strains differ from those in B. thetaiotaomicron (MK-10 and MK-11), although it is reported that the latter does also contain MK-8 and MK-9 as minor components (Shah & Collins, 1980). Our strains are sensitive to bile acids, whereas the related Bacteroides species are resistant. Our strains also differ from the three most closely related species in terms of other properties such as indole production and acid production from various saccharides. It is reported that the major CFAs of species in the Bacteroides–Prevotella group are anteiso-C15 : 0, iso-C15 : 0, iso-C17 : 0 3-OH and C16 : 0 (Miyagawa et al., 1979; Moore et al., 1994). Although the CFA compositions of strains SV434T and S562 differed somewhat from each other, the overall pattern, with anteiso-C15 : 0 and iso-C15 : 0 as major components, seems to correspond with that reported for Bacteroides species.
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). Growth of strains SV434T and S562 was also strongly stimulated by the addition of haemin to the medium. Recently we described three novel species from the phylum Bacteroidetes (relating to the Bacteroides–Prevotella group) that had been isolated from plant residue from an irrigated rice field in Japan. Two of these three species also required haemin for growth (Ueki et al., 2006a, b, 2007). These results strongly suggested that major bacterial species relating to the Bacteroides–Prevotella group living in natural habitats other than animal bodies might also require haemin for growth. Catalase activity is not usually detected in Bacteroides species, though it is known that catalase production in B. thetaiotaomicron is variable depending on the strain (Holdeman et al., 1984) and that the presence or absence of haemin in the culture medium affects the production of catalase of some species in the Bacteroides–Prevotella group (Wilkins et al., 1978). Cells of strains SV434T and S562 also showed catalase production that was variable in response to the presence or absence of haemin in the medium. Strains SV434T and S562 were isolated from a methanogenic reactor. Although both strains share some features with Bacteroides species, such as a haemin requirement, the G+C content of the genomic DNA and the CFA profile, they showed various unique characteristics that served to differentiate them from known Bacteroides species. The fact that the optimum growth temperature of SV434T and S562 is 30 °C and that they do not grow at 37 °C indicate that they have adapted to non-mammalian environments, i.e. the novel strains are not derived from cattle. The sensitivity to bile acids and the slightly alkaliphilic nature of the strains also seem to support an ecological specificity that differentiates them from Bacteroides species derived from mammalian bodies.
Most Bacteroides species produce acetate and succinate as major products from glucose; species that produce propionate as a major end product are less common. Strains SV434T and S562 require cobalamin in addition to haemin for growth and produce abundant amounts of propionate. The methylmalonyl-CoA pathway, a major pathway involved in propionate production, is dependent on cobalamin, so it was clear that our strains were producing propionate with a pathway dependent on an exogenous supply of cobalamin. It is known that exogenous cobalamin is required for propionate production from succinate in Bacteroides fragilis (Holdeman et al., 1984). We recently described two novel species of anaerobic bacteria isolated from plant residue in irrigated rice-field soil and which produced propionate in a manner that was dependent upon an exogenous supply of cobalamin (Akasaka et al., 2003b; Ueki et al., 2006b). Cobalamin requirements in bacterial species that produce propionate seem to be rather common in anaerobes, irrespective of the habitat. The fact that cobalamin and haemin could be replaced by the clarified sludge fluid obtained from the methanogenic reactor indicates that the growth of these bacteria (which have complex nutritional requirements) is readily supported by exogenous growth factors present in the environment.
In addition to the phylogenetic distances involved, the obvious physiological differences suggest that strains SV434T and S562 represent a novel Bacteroides species with an ecological function that differs significantly from those of Bacteroides species that live in mammalian bodies. Recently, it was proposed that the presence of species from the Bacteroides–Prevotella group represents a novel indicator of faecal contamination in the environment (Bernhard & Field, 2000). Our data, together with other reports showing the presence of such species in various natural habitats, indicate that the distribution of members of the group in non-animal environments should be investigated more carefully and extensively.
On the basis of the above-mentioned comprehensive analyses of the phylogenetic, phenotypic and chemotaxonomic characteristics (and ecological/functional properties) of the two isolates, SV434T and S562 represent a novel species of the genus Bacteroides, for which the name Bacteroides propionicifaciens sp. nov. is proposed.
Description of Bacteroides propionicifaciens sp. nov.
Bacteroides propionicifaciens (pro.pi.on.i.ci.fa'ci.ens. N.L. n. acidum propionicum propionic acid; L. v. facio make; N.L. part. adj. propionicifaciens propionic acid-producing).
Cells are Gram-negative, non-motile, non-spore-forming rods (0.7–0.8 µm wide and 1.3–2.1 µm long, with some longer cells). Long, filamentous rods often occur. Remarkable stimulation of growth is produced by the addition of haemin and cobalamin (vitamin B12) to the medium. Utilizes arabinose, fructose, galactose, glucose, mannose, cellobiose, maltose, glycogen, starch, dextrin, amygdalin, lactate and pyruvate. Produces acetate and propionate and a small amount of succinate in the presence of haemin and cobalamin from the substrates used. Lactate is also produced in the absence of haemin. Utilizes lactose, aesculin and fumarate weakly. Does not utilize ribose, xylose, rhamnose, sorbose, melibiose, sucrose, trehalose, melezitose, raffinose, CM-cellulose, cellulose powder, filter paper, xylan, pectin, inulin, salicin, glycerol, dulcitol, inositol, mannitol, sorbitol, ethanol, malate or succinate. Slightly alkaliphilic; optimum pH is about 7.9. Growth temperature range is 5–35 °C; optimum is 30 °C. NaCl concentration range for growth is 0–4.0 % (w/v); optimum is 1.0 % (w/v) NaCl in PYHVG medium. Catalase activity is not usually detected in cells cultivated without haemin; cells cultivated with haemin usually show catalase activity. Does not show oxidase, nitrate-reducing or urease activities. Does not produce hydrogen sulfide or indole. Hydrolyses aesculin but not gelatin. Sensitive to bile acids. The major cellular fatty acids are anteiso-C15 : 0 and iso-C15 : 0. MK-8(H0) and MK-9(H0) are the major respiratory quinones and the genomic DNA G+C content is 46.2–47.5 mol%.
The type strain, SV434T (=JCM 14649T =DSM 19291T), was isolated from rice-straw residue from a methanogenic reactor treating waste from cattle farms. Reference strain S562 (=JCM 14650 =DSM 19346) was isolated from the same reactor.
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ACKNOWLEDGEMENTS |
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