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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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Present address: Creative Research Initiative ‘Sousei’ (CRIS), Hokkaido University, Kita 21, Nishi 10, Kita-ku, Sapporo 001-0021, Japan. 
Present address: Graduate School of Agriculture, Hokkaido University, Kita 9, Nishi 9, Kita-ku, Sapporo 060-8589, Japan.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains KB7T and A42 are AB078827 and AB081578, respectively.
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; Wassmann et al., 2000). Diverse fermentative bacterial groups play a key role in decomposition of organic matter, including plant residue such as rice straw, stubble and roots ploughed into the anoxic rice-field soil, thus producing methanogenic substrates such as acetate, formate and H2. Living plant roots also provide growth substrates for microbes either by secreting organic matter such as saccharides, amino acids and organic acids or from cellular material peeling off the root epidermis and cortex (Kaku et al., 2000). Methane produced from decomposition of these substrates is emitted to the atmosphere as one of the major greenhouse gases (Takai, 1970; Seiler et al., 1984; Boone, 2000; Khalil, 2000; Wassmann et al., 2000).
Various fermentative anaerobes from samples of rice plant residue and living rice roots from irrigated rice-field soil have been isolated during the course of our investigations from microbes in anoxic rice-field soil (Satoh et al., 2002; Akasaka et al., 2003a, 2004). Of the isolates from rice plant residue, three novel propionate-producing species in the phyla Actinobacteria and Bacteroidetes have been described recently (Akasaka et al., 2003b; Ueki et al., 2006a, b). In this study, two other strains that are phylogenetically distant from any related recognized species have been isolated from rice plant residue and living rice roots and characterized. The isolates were strictly anaerobic, xylanolytic bacteria consisting of Gram-negative, non-motile rod-like cells. Although all recognized species in the genus Prevotella have been isolated from mammalian sources such as human oral, urogenital or other clinical sources and the rumen, it is proposed that the two strains isolated here (KB7T and A42) should be accommodated in the genus Prevotella as a novel species based on the comprehensive characterization carried out.
Strain KB7T (=JCM 13650T=DSM 17968T) was isolated from a plant residue sample (rice stubble and roots) collected from irrigated rice-field soil in the Shonai Branch of the Yamagata Agricultural Experimental Station (Tsuruoka, Yamagata, Japan) during the flooding period of the field in June 1994 (Akasaka et al., 2003a). Strain A42 (=JCM 13651=DSM 17969) was isolated from roots of living rice plants in the same field in August 1993 during the period of intermittent irrigation (Satoh et al., 2002). Cultivation practices for rice plants and other field conditions have been described previously (Ueki et al., 2000). Samples homogenized by a Waring blender (10 000 r.p.m., 10 min.) under N2 gas were used for isolation (Satoh et al., 2002; Akasaka et al., 2003a, 2004). Strains were isolated by the anaerobic roll tube method for enumeration of anaerobic fermentative bacteria using the colony-counting method (Hungate, 1966; Holdeman et al., 1977).
The strains were cultivated anaerobically at 30 °C unless otherwise stated by using peptone–yeast extract (PY) medium as basal medium with O2-free 95 % N2/5 % CO2 mixed gas in the headspace as described by Akasaka et al. (2003a, b). PY medium supplemented with (l–1) 0.25 g each of glucose, cellobiose, maltose and soluble starch plus 15 g agar (Difco) was designated PY4S agar and used for isolation and maintenance of the strain 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 the B-vitamin mixture (10 ml l–1) (PYHV medium) as well as 10 g glucose l–1 (PYHVG medium) were used for cultivation of the strains for various physiological tests and chemotaxonomic analyses of the cells unless otherwise stated (Ueki et al., 2006b). 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 strains 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 resazurin in the 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 10 g l–1 (for sugars and sugar alcohols) or 30 mM (organic acids). Bile sensitivity was determined by the addition of bile salts (0.1–0.5 %, w/v; Oxoid) 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 methods described by Holdeman et al. (1977) and Ueki et al. (2006a, b).
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 an HP Ultra2 column. CFAs were identified by equivalent chain-length (Miyagawa et al., 1979; Ueki & Suto, 1979) according to the protocol of TechnoSuruga (Shimidu, Japan), based on the MIDI Microbial Identification System (Microbial ID; Moore et al., 1994). The TSBA40 microbial identification system was also used to confirm identification. Isoprenoid quinones were extracted as described by Komagata & Suzuki (1987) and analysed by MS (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 GC kit (Yamasa shoyu) and its G+C content was measured by HPLC (Hitachi L-7400) equipped with a µBondapack C18 column (3.9x300 mm; Waters).
DNA extraction and PCR amplification were performed according to the method described by Akasaka et al. (2003a). The 16S rRNA gene was PCR amplified using the 27f and 1492r primer set and sequenced by using a ThermoSequenase 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 program BLAST (Altschul et al., 1997). A phylogenetic tree was constructed with the neighbour-joining method (Saitou & Nei, 1987) by using the program CLUSTAL W (Thompson et al., 1994). All gaps and unidentified base positions in the alignments were excluded before sequence assembly.
Cellular and various physiological characteristics were determined for strains KB7T and A42 and they showed almost the same phenotypic properties. Of the physiological characteristics of both strains shown below, detailed descriptions such as growth rates and amounts of products were based mainly on data from strain KB7T as the representative strain.
Cells of both strains were Gram-negative rods, 0.7–0.8 µm in width and 1.3–2.1 µm in length with some longer (4.0–12.0 µm) cells (Fig. 1). Cells were non-motile as observed by phase-contrast microscopy. Colonies on PY4S agar were translucent and thin with a smooth surface. Neither strain could grow in air on PY4S or nutrient agar. Spore formation was not observed and cells treated at 80 °C for 10 min did not grow. Catalase and oxidase activities were not detected.
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). Further addition of vitamin K to the medium did not seem to affect the growth rate. Although addition of the B-vitamin mixture did not stimulate growth, it seemed to bring about stable growth behaviour of the strains. Thus, physiological characteristics of the strains were usually determined in the presence of B-vitamin mixture plus haemin (PYHV medium). Cells for chemotaxonomic characterization were also cultivated in the presence of these growth factors (PYHVG medium). Both strains utilized arabinose, xylose, fructose, galactose, glucose, mannose, rhamnose, cellobiose, lactose, maltose, sucrose, carboxymethylcellulose (CMC), soluble starch, xylan, pectin and salicin as growth substrates. Ribose, pyruvate and fumarate were utilized weakly. Acids were produced from all substrates utilized, but gas was not. The strains did not use sorbose, trehalose, melezitose, cellulose powder, filter paper, inulin, glycerol, inositol, mannitol, lactate, malate or succinate.
Fermentation products in PYG medium (without haemin and vitamins) were acetate (2.6 mM), succinate (4.1 mM) and malate (5.9 mM), whereas in the presence of haemin and vitamins (PYHVG medium), both strains produced acetate (9.2 mM) and succinate (15.9 mM) as major acids with lower amounts of formate (2.6 mM) and malate (0.4 mM). Almost the same amounts of acetate and succinate were produced from the other substrates tested, including xylan and pectin. Acid production from CMC was rather weak (3.4 mM acetate and 6.1 mM succinate). Products from fumarate were acetate (3.9 mM), succinate (6.6 mM), malate (8.8 mM) and a trace amount of formate; products from pyruvate were formate (3.9 mM), acetate (8.9 mM), succinate (4.1 mM) and a trace amount of malate. Aesculin was hydrolysed, but gelatin was not. The strains were negative for the production of urease, hydrogen sulfide and indole. They did not reduce nitrate and could not grow in the presence of 0.1 % (w/v) bile salts.
The strains grew at pH 4.7–7.6, with optimum growth at pH 5.7–6.7, a rather wide pH range for optimum growth. The final pH of the PYHVG medium was about pH 4.5. The temperature range for growth was 10–40 °C, with optimum growth at 30 °C. The growth rate at 37 °C (µ=0.35 h–1) was rather high, but it dropped sharply to a much lower level at 40 °C (µ=0.071 h–1). The growth rate at 10 °C was 0.019 h–1. The NaCl concentration range for growth was 0–1.0 % (w/v).
The major CFAs of strain KB7T were anteiso-C15 : 0 (27.3 %), iso-C15 : 0 (11.9 %), C15 : 0 (10.1 %), iso-C17 : 0 3-OH (9.1 %), iso-C14 : 0 (7.9 %) and C16 : 0 3-OH (6.8 %), with lower amounts of iso-C13 : 0 (4.4 %), C14 : 0 (3.9 %), iso-C16 : 0 3-OH (3.9 %) and C16 : 0 (3.3 %). Unsaturated fatty acids were not detected. The predominant respiratory quinones of strain KB7T were menaquinones MK-11 and MK-11(H2). The genomic DNA G+C content was 39.2 mol%. These chemotaxonomic analyses were not carried out for strain A42.
The similarity between the 16S rRNA gene sequences of strains KB7T and A42 was 99.8 % and both strains were assigned to the phylum Bacteroidetes (Garrity & Holt, 2001). The closest relative to both strains in the GenBank database was Prevotella sp. HY-36-2 (AY581270) with sequence similarity of 98.7–99.0 %. Of species with validly described names, the species most closely related to both strains all belonged to the genus Prevotella, i.e. Prevotella oulorum ATCC 43324T (Shah et al., 1985; 92.8–92.9 % similarity), Prevotella veroralis ATCC 33779T (Watabe et al., 1983; 92.0–92.4 %) and Prevotella melaninogenica ATCC 25845T (Holdeman et al., 1984; 91.9–92.0 %). The next most closely related species were Prevotella corporis and Prevotella bryantii (Holdeman et al., 1984; Avgustin et al., 1997; 91.1–92.0 % similarity). Strains KB7T and A42 formed a separate branch from related Prevotella species in the phylogenetic tree composed of all recognized Prevotella species (Fig. 2).
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, 1990; Paster et al., 1994) including recently described species (Sakamoto et al., 2004, 2005a, b; Berger et al., 2005; Downes et al., 2005, 2006), with the exception of species isolated from the rumen (Avgustin et al., 1997). Thus, the habitats of strains KB7T and A42 are extremely different, i.e. rice plant residue in flooded rice-field soil and living rice roots, from those of currently known Prevotella species. The optimum growth temperature of the strains is 30 °C and they grow only weakly at 40 °C; thus, the temperature of mammals at around 37 °C is near the upper limit for growth of both strains.
Many species in the genus Prevotella have a requirement for haemin for growth; the closest relatives of strains KB7T and A42 also require haemin for growth or they are usually cultivated in the presence of haemin (Holdeman et al., 1984; Shah et al., 1985). Growth of our strains was also strongly stimulated by the addition of haemin to the medium. Xylanibacter oryzae strain KB3T, isolated from plant residue in the same rice field as strain KB7T, also requires haemin for growth (Ueki et al., 2006b).
Some characteristics of strain KB7T, as representative strain, were compared with those of the three most closely related known species (P. oulorum, P. veroralis and P. melaninogenica) (Table 1). Substrates that can be utilized by these related species are relatively limited; these species are not able to utilize pentoses (arabinose and xylose), rhamnose or salicin, which are utilized by strains KB7T and A42. Furthermore, the two isolates utilized polysaccharides such as xylan, pectin and CMC, whereas the related species did not utilize these polymers except for xylan-utilizing P. veroralis. In addition, KB7T, A42 and P. veroralis utilized cellobiose, whereas the other two species did not.
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; Shah et al., 1985).
The G+C content of genomic DNA of strain KB7T (39.2 mol%) is close to those of P. veroralis (42.1 mol%) and P. melaninogenica (36–40 mol%) and slightly lower than that of P. oulorum (45–46 mol%) (Watabe et al., 1983; Holdeman et al., 1984; Shah et al., 1985). Many Prevotella species have menaquinone MK-11 as one of the predominant menaquinones (Shah & Collins, 1980) and strain KB7T possesses menaquinones MK-11 and MK-11(H2). Although the presence of hydrogenated menaquinone, MK-11(H2), is rather rare in Prevotella species (Shah & Collins, 1980; Sakamoto et al., 2005a), strain KB7T and related Prevotella species do share a common menaquinone.
It has been reported that the major CFAs in species of the two genera Bacteroides and Prevotella are anteiso-C15 : 0, iso-C15 : 0, iso-C17 : 0 3-OH and C16 : 0 (Miyagawa et al., 1979; Moore et al., 1994). Although C16 : 0 is only a minor component of CFAs of strain KB7T, the overall pattern of the CFA composition with anteiso-C15 : 0 and iso-C17 : 0 3-OH as major components seems to have a common profile to those reported for Bacteroides and Prevotella species. However, the CFA composition of strain KB7T is actually rather different from that of P. oulorum in the levels of some CFAs such as C15 : 0 and iso-C17 : 0 (Shah et al., 1985). Furthermore, although P. veroralis and P. melaninogenica have an unsaturated fatty acid (C18 : 1) as one of the most dominant CFAs (17.2 and 17.9 %, respectively) (Sakamoto et al., 2004), strain KB7T does not contain unsaturated fatty acids (Table 2).
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) and strain A42 was isolated from living rice roots as one of the predominant culturable anaerobic bacteria (Satoh et al., 2002). Hemicellulose together with cellulose and lignin make up the major polymeric constituents of plant cell walls. Hemicellulose is a heteropolysaccharide composed of various sugars such as xylose, arabinose, glucose, galactose and mannose. Xylan is composed of xylose and constitutes the major component of hemicellulose (Collins et al., 2005). Pectin also occurs in the primary cell walls and intercellular regions of plants. It is known that pectin, which is a complex polysaccharide composed mainly of galacturonic acid, usually contains rhamnose residues as important components. Strains KB7T and A42 both utilized these plant polymers (xylan, pectin and CMC) as well as the major components of the polymeric constituents. Both strains also utilized cellobiose, which is generated by hydrolysis of cellulose. Thus, it was strongly suggested that the bacterial group related to strains KB7T and A42 should take an important part in decomposition of the plant cell wall, especially hemicellulose and pectin, including intermediate substrates derived from the decomposition of plant cell walls. The isolation of strain A42 from living rice roots indicates that the bacterial group colonizes rice roots before harvesting of rice and plays an important role in the decay of rice roots in rice-field soil.
Strains KB7T and A42 have some features in common with those of related Prevotella species as shown above, although these related species are all isolated from human clinical specimens and all known species in the genus Prevotella are derived from mammalian sources (Fig. 2
). In addition to low 16S rRNA gene sequence similarities, the obvious ecological difference suggests that strains KB7T and A42 should represent a novel species in the genus Prevotella, having a significantly different ecological function from those Prevotella species living in mammals.
On the basis of the above-mentioned comprehensive analyses of the phylogenetic, phenotypic and chemotaxonomic characteristics, as well as the ecological and functional properties, the novel species Prevotella paludivivens sp. nov. is proposed to accommodate strains KB7T and A42.
Description of Prevotella paludivivens sp. nov.
Prevotella paludivivens (pa.lu.di.vi'vens. L. n. palus, -udis swamp, marsh; L. v. vivo to live; N.L. part. adj. paludivivens living in swamps).
Cells are Gram-negative, non-spore-forming, non-motile, short rods. Strictly anaerobic. Chemo-organotroph. Haemin significantly stimulates growth. pH optimum for growth is 5.7–6.7. Temperature range for growth is 10–40 °C, with optimum growth at 30 °C. Growth at 37 °C is delayed compared with that at 30 °C. NaCl concentration range for growth is 0–1.0 % (w/v) in PYG medium. Oxidase, catalase and nitrate-reducing activities are not detected. Utilizes arabinose, ribose, xylose, fructose, galactose, glucose, mannose, rhamnose, cellobiose, lactose, maltose, sucrose, CMC, soluble starch, xylan, pectin and salicin as growth substrates and produces acetate and succinate as major fermentation end products. Gas is not produced. Pyruvate and fumarate are also utilized. Does not use sorbose, trehalose, melezitose, cellulose powder, filter paper, inulin, glycerol, inositol, mannitol, lactate, malate or succinate. Hydrolyses aesculin, but not gelatin. Urease-negative. Hydrogen sulfide and indole are not produced. Does not grow in the presence of bile salts. The major cellular fatty acids are anteiso-C15 : 0, iso-C15 : 0, C15 : 0 and iso-C17 : 0 3-OH. Major respiratory quinones are MK-11 and MK-11(H2).
The type strain is KB7T (=JCM 13650T=DSM 17968T), isolated from rice plant residue in flooded rice-field soil; the genomic DNA G+C content of strain KB7T is 39.2 mol%. Strain A42 (=JCM 13651=DSM 17969) is a reference strain derived from rice roots of living rice plants.
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ACKNOWLEDGEMENTS |
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We thank Dr. K. Takahashi for his technical advice on the analysis of isoprenoid quinones.
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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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