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Faculty of Agriculture, Yamagata University, Wakaba-machi 1-23, Tsuruoka 997-8555, Japan
Correspondence
Atsuko Ueki
uatsuko{at}tds1.tr.yamagata-u.ac.jp
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain KB3T is AB078826.
Present address: Creative Research Initiative ‘Sousei’ (CRIS), Hokkaido University, Kita 21, Nishi 10, Kita-ku, Sapporo, 001-0021, Japan. 
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; Seiler et al., 1984; Boone, 2000; Khalil, 2000; Wassmann et al., 2000a, b).
During the course of an investigation into microbes in anoxic rice-field soil, we have isolated various fermentative anaerobes from samples of rice-plant residue, as well as living rice roots, in irrigated rice-field soil (Satoh et al., 2002; Akasaka et al., 2003a, 2004). We have previously described two novel anaerobic, propionate-producing species that were isolated from rice straw samples (Akasaka et al., 2003b; Ueki et al., 2006). In this study, a novel strain, KB3T, one of a group of isolates from stubble and roots that were phylogenetically distant from any related recognized species, was characterized. The novel isolate was a strictly anaerobic, xylanolytic and propionate-producing bacterium consisting of Gram-negative, non-motile rod-like cells. Based on phylogenetic, ecological, physiological and chemotaxonomic characteristics, we propose a novel genus and species in the phylum Bacteroidetes to accommodate strain KB3T.
Strain KB3T was isolated from a sample of rice-plant residue (rice stubble and roots) collected from irrigated rice-field soil at the Shonai Branch of the Yamagata Agricultural Experimental Station (Tsuruoka, Yamagata, Japan) during the flooding period of the field. Cultivation practices for rice plants and other conditions of the fields have been described previously (Ueki et al., 2000). The strain was isolated by the anaerobic roll tube method for the enumeration of anaerobic fermentative bacteria by the colony-counting method (Hungate, 1966; Holdeman et al., 1977). Plant residue samples (rice stubble and roots) homogenized using a Waring blender (10 000 r.p.m., 10 min) under N2 gas were used as sources for the isolation of novel strains (Akasaka et al., 2003a, 2004).
The novel strain was cultivated anaerobically at 30 °C unless otherwise stated. Peptone-yeast extract (PY) medium was used as the basal medium with oxygen-free, 95 % N2/5 % CO2 mixed gas as the headspace as described by Akasaka et al. (2003a). PY medium supplemented with (l–1) 0.25 g glucose, cellobiose, maltose and soluble starch and 15 g agar (Difco) was designated PY4S agar and used for the maintenance of the novel strain in agar slants. For the cultivation of the strain for various physiological tests and chemotaxonomic analyses, PYHV medium [PY liquid medium supplemented with haemin (at a final concentration of 5 mg l–1; Holdeman et al., 1977) and B-vitamin mixture (10 ml l–1)] and PYHVG medium (PYHV medium supplemented with 10 g glucose l–1) were used, unless otherwise stated. Since strain KB3T was slightly acidophilic, as described below, the pH of liquid media was usually adjusted to about pH 6.0. The composition of the B-vitamin mixture used was (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 by changes in OD660.
Growth of the novel strain under aerobic conditions was examined by plate culture on nutrient agar (Nissui Pharmacy) and PY4S agar modified to exclude Na2CO3, cysteine-HCl-H2O and sodium resazurine in PY basal medium. Spore formation was assessed by observation of cells after Gram-staining and by growth of cells exposed to 80 °C for 10 min. Oxidase, catalase and nitrate-reducing activities were determined according to methods described by Satoh et al. (2002) and Akasaka et al. (2003a, b). Utilization of carbon sources was tested in PYHV liquid medium with each substrate added at a concentration of 10 g l–1 (for sugars and sugar alcohols) or 30 mM (organic acids). Bile sensitivity was determined by the addition of bile salts (Oxoid; 0.1–0.5 %, w/v) to PYHVG and PYG media (Lawson et al., 2002). 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. (2006).
Whole-cell fatty acids (CFAs) were converted to methyl esters according to the method of Miller (1982). Methyl esters of CFAs were analysed by GC (HP6890; Hewlett Packard or G-3000; Hitachi) equipped with a HP Ultra2 column. CFAs were identified by equivalent chain-length (ECL) (Miyagawa et al., 1979; Ueki & Suto, 1979) according to Moore's protocol of NCIMB Japan based on the MIDI microbial identification system (Microbial ID) (Moore et al., 1994). The microbial identification system of the TSBA40 was also used for confirmation of identification. Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and analysed by using a mass spectrometer (JMS-SX102A; JEOL). Genomic DNA was extracted according to the method of Kamagata & Mikami (1991). Extracted DNA was digested with P1 nuclease by using a Yamasa GC kit (Yamasa shoyu) and the DNA G+C content was measured by HPLC (L-7400; Hitachi) equipped with a µBondpack C18 column (3.9x300 mm; Waters).
DNA extraction and PCR amplification were performed according to the method described by Akasaka et al. (2003a). 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). 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 CLUSTAL W (Thompson et al., 1994). All gaps and unidentified base positions in the alignments were excluded before sequence assembly.
Cells of strain KB3T were Gram-negative rods. The strain grew very slowly in PYG liquid medium without haemin. The addition of haemin to the medium greatly enhanced growth as described below and the morphology of the cells was significantly altered depending on the growth medium. Most of the cells grown in the presence of haemin were short rods (0.6–0.7x2.2–2.6 µm) with some longer rods (4–10 µm) (Fig. 1a), while cells grown on PY4S agar slants (without haemin) often occurred as filamentous rods (20–50 µm long) with some chains of cells (Fig. 1b). Cells were non-motile as observed by phase-contrast microscopy. Colonies on PY4S agar were translucent and thin with a smooth surface and were 0.5–0.8 mm diameter after 3–4 days of incubation. The novel strain could not grow in air either on PY4S or nutrient agar. Spore formation was not observed and cells treated at 80 °C for 10 min did not grow.
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When cells were cultivated to the stationary growth phase in the presence of haemin and then used as an inoculum for growth experiments, the growth of the strain was often found to be considerably delayed, irrespective of the haemin concentration of the medium. Thus, the viability or culturability of the cells grown in the presence of haemin appeared to be significantly reduced early in the stationary phase. Thus, for stable and reproducible growth experiments, it was essential to use cells in the late-exponential or early-stationary growth phase. Cells cultivated without haemin did not show any significant decline of viability, even at the stationary phase. Thus, PY4S agar, a medium without haemin, was usually used for the maintenance of the novel strain as slant cultures.
Both catalase and oxidase activities were negative and the novel strain did not reduce nitrate. Strain KB3T utilized arabinose, ribose, xylose, fructose, galactose, glucose, mannose, rhamnose, cellobiose, lactose, maltose, sucrose, trehalose, carboxymethylcellulose (CMC), soluble starch, xylan, pectin, salicin and pyruvate as growth substrates. Acids were produced from all substrates used, but gas was not. Strain KB3T did not use sorbose, melezitose, cellulose powder, filter paper, inulin, glycerol, inositol, mannitol, fumarate, lactate, malate or succinate.
The major products of the novel strain in PYHG medium were acetate and succinate. Propionate production was significantly stimulated in the presence of the B-vitamin mixture (Table 1). Strain KB3T also produced substantial amounts of acetate, propionate and succinate from xylan and, with this substrate, propionate production was also significantly stimulated by the addition of the B-vitamin mixture. The B-vitamin mixture could be completely replaced by cyanocobalamin at the same concentration as in the vitamin mixture (final concentration of 10 µg l–1). Propionate was also a major product from pectin, CMC and pyruvate in the presence of the vitamin mixture, while succinate was a minor product. A small amount of malate was usually detected. Formate was not detected from any of the substrates examined.
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Strain KB3T was slightly acidophilic with the optimum pH at 5.7–6.2 and a pH range of 4.7–7.3 for growth. Even at an initial pH of 7.3, growth was significantly delayed. When the novel strain was grown in PYHVG medium at an initial pH of 6.1, the final pH was 4.1. The temperature range for growth was 10–37 °C, with an optimum temperature of 30 °C. The growth rate at 37 °C (µ=0.194 h–1) was significantly lower than that at 30 °C (0.29–0.33 h–1) and the strain could not grow at 37 °C in the absence of haemin. The NaCl concentration range for growth was 0–0.5 % (w/v).
The major CFAs of strain KB3T were anteiso-C15 : 0 (42.2 %) and iso-3-OH C17 : 0 (21.8 %), with lower amounts of 3-OH C17 : 0 (5.2 %), C15 : 0 (4.7 %), anteiso-3-OH C17 : 0 (3.7 %), iso-C15 : 0 (3.7 %), iso-C17 : 0 (3.3 %) and C16 : 0 (3.1 %). Unsaturated fatty acids were not detected. The predominant respiratory quinones of the strain were menaquinones MK-12(H2) and MK-13(H2). The G+C content of genomic DNA was 43.6 mol%.
Strain KB3T was assigned to the phylum Bacteroidetes (Garrity & Holt, 2001) based on the 16S rRNA gene sequence (Fig. 2). The closest recognized species to strain KB3T was Prevotella bivia ATCC 29303T (originally described as Bacteroides bivius) (Holdeman & Johnson, 1977; Holdeman et al., 1984) with a gene sequence similarity of 89.5 %. Prevotella albensis DSM 11370T (formerly Bacteroides ruminicola subsp. ruminicola biovar 7) (Holdeman et al., 1984; Avgustin et al., 1997) and Prevotella oulorum ATCC 43324T (Shah et al., 1985) were the next most closely related species (both with gene sequence similarity of 89.1 %). The fourth and fifth most closely related species were also species of the genus Prevotella (Prevotella corporis and Prevotella loescheii, with 88.8 and 88.7 % gene sequence similarity, respectively) (Holdeman et al., 1984). The species found to be most closely related to strain KB3T are all isolates from mammalian species, including the urogenital region of humans (P. bivia), rumen (P. albensis), oral cavities of humans (P. oulorum and P. loescheii) and other human clinical specimens (P. corporis) (Holdeman et al., 1984; Shah et al., 1985).
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. Phylogenetic analysis revealed that strain KB3T showed 16S rRNA gene sequence similarity values of less than 90 % with the closest recognized species. The genus Prevotella mainly consists of species from human oral or urogenital sources with important exceptions isolated from rumen, such as P. ruminicola, P. albensis, Prevotella brevis and Prevotella bryantii (Shah & Collins, 1989, 1990; Paster et al., 1994; Avgustin et al., 1997). Strain KB3T was isolated from a very different environment, rice-plant residue from anoxic rice-field soil, from the known habitats of the recognized Prevotella species. The optimum growth temperature of strain KB3T at 30 °C may reflect the different environmental source of this strain compared with other related species. In addition to the low 16S rRNA gene sequence similarity values, the obvious ecological difference strongly indicates that strain KB3T represents a novel taxon in the phylum Bacteroidetes that inhabits anaerobic environments other than mammals.
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; Shah et al., 1985). Growth of strain KB3T was also strongly stimulated by the addition of haemin to the medium. Since the haemin requirement of Prevotella species has often been considered in relation to haem or haemoglobin derived from host animals (Leung & Folk, 2002), it is of interest that haemin also stimulates the growth of a bacterium isolated from a plant residue sample in flooded soil. Although cells of Prevotella or Bacteroides species are often known to be pleomorphic depending on the culture conditions (Holdeman et al., 1984), the morphology of long filamentous rods cultivated in the absence of haemin seems to be a unique feature of strain KB3T together with the slightly acidophilic property.
The ranges of substrate utilization of the related species P. bivia and P. oulorum are relatively restricted and these species are not able to utilize carbohydrates such as arabinose, xylose and cellobiose. Furthermore, utilization of polymers such as xylan, pectin and CMC is never reported. Strain KB3T is able to use various carbohydrates, including polymers (xylan, pectin, CMC and starch) and disaccharides (e.g. cellobiose, trehalose and sucrose), as well as hexoses and pentoses, including arabinose and xylose. P. albensis, isolated from rumen, utilizes a relatively wide range of carbohydrates, including xylose and xylan, which were key characteristics used to divide Bacteroides ruminicola into subspecies (B. ruminicola subsp. ruminicola and B. ruminicola subsp. brevis) (Holdeman et al., 1984). P. albensis, established from the former subspecies, is reported to utilize pectin strongly as well as arabinose and cellobiose. Thus, strain KB3T has characteristics common to Prevotella species isolated from rumen as regards the utilization of polymers, however, the range of carbohydrate utilization of strain KB3T is different from that of P. albensis (e.g. mannose, sucrose, trehalose and CMC) (Table 1
).
P. bivia and P. oulorum produce acetate and succinate as major acids from glucose and production of propionate has never been reported. For P. albensis, the major acids from glucose are succinate, acetate and formate. Propionate is not recognized as a major acid (Holdeman et al., 1984; Shah et al., 1985). Strain KB3T produced a substantial amount of propionate from xylan, irrespective of the presence of haemin. In the presence of the B-vitamin mixture, propionate was usually the major end product from the substrates tested. Since the vitamin mixture could be completely replaced by cyanocobalamin, strain KB3T is considered to be a propionate-producing bacterium depending on the supply of exogenous cobalamin. A propionate-producing bacterium, Propionicimonas paludicola, which requires cobalamin for growth and propionate production also has been isolated from rice-plant residue samples from the same rice-field (Akasaka et al., 2003b). The requirement for cobalamin for the production of propionate seems to be a rather common physiological characteristic of anaerobic bacteria living in anoxic environments such as flooded soil.
The G+C content of the genomic DNA of strain KB3T (43.6 mol%) is similar to those of related species (Table 2) (Holdeman et al., 1984; Shah et al., 1985). It has been reported that the major CFAs of species in the genera Bacteroides and Prevotella are anteiso-C15 : 0, iso-C15 : 0, iso-3-OH C17 : 0 and C16 : 0 (Miyagawa et al., 1979; Moore et al., 1994). Although iso-C15 : 0 and C16 : 0 were only minor components of the CFAs for strain KB3T, the overall pattern of the CFA content with anteiso-C15 : 0 and iso-3-OH C17 : 0 as major components seems to be within the variation of those reported for species of the genera Bacteroides and Prevotella. However, since the closest relative of strain KB3T, P. bivia, has unsaturated fatty acid (C18 : 1) as the dominant CFA (18.9 %) together with anteiso-C15 : 0 (16.9 %) and iso-3-OH C17 : 0 (17.9 %) as major CFAs (Sakamoto et al., 2004), the CFA composition of strain KB3T is rather different from that of its closest relative.
P. bivia possesses menaquinones MK-9 (5 %), MK-10 (70 %) and MK-11 (23 %) (Sakamoto et al., 2005) and P. oulorum has MK-10 (Shah et al., 1985). Prevotella species from rumen usually have menaquinone MK-11 as one of predominant menaquinones (Shah & Collins, 1980). Since strain KB3T possesses menaquinones MK-12(H2) and MK-13(H2), the menaquinone composition is rather different from those of related Prevotella species.
Strain KB3T was isolated from rice-plant residue (plant stubble and roots) together with some very closely related strains [strains KB10 (=JCM 13649=DSM 17971), KB11 and KB13; GenBank 16S rRNA gene sequence accession numbers AB07880, AB078831 and AB078833, respectively] (Akasaka et al., 2003a) (Fig. 2). The population density of this bacterial group, determined by the dilution-colony-counting method, was enumerated at the order of 109 c.f.u. g–1 dry weight. Thus, this bacterial group seems to be one of the dominant groups living in plant residues in rice-field soil and has functions in decomposing plant biomass, such as hemicellulose and pectin, as well as substrates derived from the decomposition of these components, including solubilized cellulose.
Strain KB3T is phylogenetically distant from the closest related species that are all derived from mammals and has characteristics that are distinct from these related species. Analyses using various environmental clones from samples isolated from sources other than animals have shown that bacterial groups belonging to the phylum Bacteroidetes are frequently detected as one of the predominant groups and most of them have never been cultivated (Lydell et al., 2004; Chouari et al., 2005). Strain KB3T may represent such an uncultured bacterial group taking a role in anaerobic decomposition of plant biomass.
On the basis of the comprehensive analyses of the phenotypic, chemotaxonomic and phylogenetic characteristics described above and its ecological origin, we propose a novel genus, Xylanibacter gen. nov., with strain KB3T representing the type strain of the type species, Xylanibacter oryzae sp. nov.
Description of Xylanibacter gen. nov.
Xylanibacter (Xy.la.ni.bac'ter. N.L. n. xylanum xylan; N.L. masc. n. bacter a rod; N.L. masc. n. Xylanibacter rod decomposing xylan).
Cells are Gram-negative, non-spore-forming, non-motile, short to filamentous rods. Strictly anaerobic. Chemo-organotroph. Optimum growth temperature is 30 °C. Oxidase, catalase and nitrate-reducing activities are negative. Utilize various sugars including xylan and produce acetate, propionate and succinate as major fermentation end products. Major cellular fatty acids are anteiso-C15 : 0 and iso-3-OH C17 : 0. Major respiratory quinones are MK-12(H2) and MK-13(H2). The type species is Xylanibacter oryzae.
Description of Xylanibacter oryzae sp. nov.
Xylanibacter oryzae (o'ry.zae. L. fem. n. oryza rice and the genus name of rice; L. gen. n. oryzae from/of rice or rice plants, referring to rice-plant residue from which the strain was isolated).
Has the following properties in addition to those given for the genus. Haemin significantly stimulates growth. In the presence of B-vitamin mixture as well as haemin, acetate, propionate and succinate are produced as major fermentation products. Slightly acidophilic and grows with an optimum pH of 5.7–6.2 (pH range, 4.7–7.3). Growth temperature range is 15–35 °C with the optimum at 30 °C. Growth at 37 °C is significantly delayed. NaCl concentration range for growth is 0–0.5 % (w/v) in PYG medium containing haemin and B-vitamin mixture. Utilizes arabinose, ribose, xylose, fructose, galactose, glucose, mannose, rhamnose, cellobiose, lactose, maltose, sucrose, trehalose, CMC, soluble starch, xylan, pectin, salicin and pyruvate as growth substrates. Acids are produced from these substrates, but gas is not. Does not use sorbose, melezitose, cellulose powder, filter paper, inulin, glycerol, inositol, mannitol, fumarate, lactate, malate or succinate. Aesculin is hydrolysed, but gelatin is not. Urease is negative. Hydrogen sulfide and indole are not produced. Does not grow in the presence of bile salts. The genomic DNA G+C content is 43.6 mol%.
The type strain, KB3T (=JCM 13648T=DSM 17970T), was isolated from stubble and roots of rice-plant residue in anoxic rice-field soil in Japan.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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D. Suzuki, A. Ueki, A. Amaishi, and K. Ueki Desulfoluna butyratoxydans gen. nov., sp. nov., a novel Gram-negative, butyrate-oxidizing, sulfate-reducing bacterium isolated from an estuarine sediment in Japan Int J Syst Evol Microbiol, April 1, 2008; 58(4): 826 - 832. [Abstract] [Full Text] [PDF]
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A. Ueki, K. Abe, N. Kaku, K. Watanabe, and K. Ueki Bacteroides propionicifaciens sp. nov., isolated from rice-straw residue in a methanogenic reactor treating waste from cattle farms Int J Syst Evol Microbiol, February 1, 2008; 58(2): 346 - 352. [Abstract] [Full Text] [PDF]
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A. Ueki, H. Akasaka, A. Satoh, D. Suzuki, and K. Ueki Prevotella paludivivens sp. nov., a novel strictly anaerobic, Gram-negative, hemicellulose-decomposing bacterium isolated from plant residue and rice roots in irrigated rice-field soil Int J Syst Evol Microbiol, August 1, 2007; 57(8): 1803 - 1809. [Abstract] [Full Text] [PDF]
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