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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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Published online ahead of print on 9 September 2005 as DOI 10.1099/ijs.0.63896-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain WB4T is AB078842.
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; Khalil, 2000; Wassmann et al., 2000a, b). Many studies have investigated the microbial communities in flooded rice-field soil (Janssen et al., 1997; Großkopf et al., 1998; Henckel et al., 1999; Hengstmann et al., 1999). In anoxic rice-field soil, diverse fermentative bacterial groups play a key role in decomposition of organic matter such as rice plant residue ploughed into the soil and exudate from roots of rice plants, thus producing substrates such as acetate and hydrogen for methanogenesis (Cicerone & Oremland, 1988; Boone, 2000; Glissmann & Conrad, 2000; Weber et al., 2001).
We have isolated various fermentative anaerobes from plant residue (rice straw and rice stubble) and living rice roots in irrigated rice-field soil in the course of investigations on microbes in this environment (Satoh et al., 2002; Akasaka et al., 2003a, b, 2004). In this study, we have characterized one of the isolates (strain WB4T) from plant residue samples (Akasaka et al., 2003a, 2004), and found it to be phylogenetically distant from any related recognized species. The isolate was a propionate-producing, strictly anaerobic bacterium with cells that were Gram-negative, non-motile rods. Physiological and chemotaxonomic characteristics supported the proposal of a novel genus and species in the phylum ‘Bacteroidetes’ to accommodate the strain.
Strain WB4T was isolated from a rice plant residue (rice straw) sample collected from irrigated rice-field soil in the Shonai Branch of the Yamagata Agricultural Experimental Station (Fujishima-machi, Yamagata, Japan) during the flooding period of the field (Akasaka et al., 2003a, 2004). Cultivation practices for rice plants and other conditions of the fields were described in Ueki et al. (2000). The strain was 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; Akasaka et al., 2003a, 2004).
The strain was cultivated anaerobically at 30 °C unless otherwise stated by using peptone/yeast extract (PY) medium as 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 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 strain in agar slants. PY liquid medium supplemented with 10 g glucose l–1 (PYG medium) was usually used for cultivation of the cells. Growth in liquid medium was monitored by changes in OD660.
Growth of the strain under aerobic conditions was examined by plate culture on nutrient agar (Nissui Pharmacy) and PY4S agar modified to exclude Na2CO3, cysteine hydrochloride and sodium resazurin. Spore formation was assessed by observation of cells after Gram-staining and by growth in PYG medium of cells exposed to 80 °C for 10 min. Oxidase, catalase and nitrate-reducing activities were determined according to the methods described by Satoh et al. (2002) and Akasaka et al. (2003a, b). Utilization of carbon sources was tested in PY liquid medium with each substrate added at 10 g–l (for sugars and sugar alcohols) or 30 mM (for alcohols and organic acids). Bile sensitivity was determined by the addition of bile salts (Oxoid) (0·1–0·5 %, w/v) to PYG medium (Lawson et al., 2002). Fermentation products were analysed by GC or HPLC as described previously (Ueki et al., 1986; Akasaka et al., 2003a). Other characterization was performed according to the methods described by Holdeman et al. (1977) and Akasaka et al. (2003a).
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 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 (ECL) (Miyagawa et al., 1979; Ueki & Suto, 1979) according to the protocol of NCIMB Japan based on the MIDI microbial identification system (Microbial ID) as described by Moore et al. (1994). The TSBA40 microbial identification library (MIDI Inc.) was used to confirm 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 its G+C content was measured by HPLC (Hitachi L-7400) equipped with a µBondpack C18 column (3·9x300 mm; Waters).
Genomic DNA was extracted and the 16S rRNA gene was amplified by PCR according to the method described by Akasaka et al. (2003a, b). 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 the CLUSTAL W program (Thompson et al., 1994). All gaps and unidentified base positions in the alignments were excluded before sequence assembly.
Cells of strain WB4T were Gram-negative, short rods, 0·5–0·6 µm in diameter and 1·3–1·7 µm in length. Ends of cells were usually round to slightly tapered (Fig. 1). Longer cells were occasionally formed both singly and in chains of the short cells. Spherical cells sometimes developed after storage of slant cultures for 1–2 months at 4 °C. Cells were non-motile as observed under phase-contrast microscopy. The strain could not grow in air on either PY4S or nutrient agar. Colonies on PY4S agar were greyish white, translucent and circular with a smooth surface and were 1–1·5 mm diameter after 48 h anaerobic incubation. When freshly cultivated cells were used as an inoculum, the strain grew rapidly in PYG liquid medium at a specific growth rate (µ) of 0·343 h–1 at 30 °C; however, inoculation from older cultures sometimes significantly delayed growth. Spore formation was not observed and cells treated at 80 °C for 10 min did not grow.
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). Aesculin was hydrolysed, but gelatin was not. Production of urease, hydrogen sulfide and indole were negative. The strain could not grow in the presence of 0·1 % (w/v) bile salts, demonstrating that it was sensitive to bile.
Temperature range for growth was 15–35 °C with an optimum at 30 °C. Even at 33 °C, the growth rate was significantly lower than that at 30 °C, and the strain could not grow at 37 °C. pH range for growth was 5·0–7·6 with an optimum at pH 6·6. NaCl concentration range for growth was 0–0·5 % (w/v) in PYG medium, but the growth rate in the presence of 
0·3 % (w/v) NaCl was much lower than that in the absence of NaCl.
The predominant CFAs of strain WB4T were anteiso-C15 : 0 (30·8 %), C15 : 0 (19·0 %), anteiso-C17 : 0 3-OH (17·9 %) and iso-C17 : 0 3-OH (6·2 %). The major respiratory quinone of strain WB4T was MK-8(H4). The G+C content of the genomic DNA was 39·3±1·0 mol%.
An almost-complete 16S rRNA gene sequence of strain WB4T assigned the strain to the phylum ‘Bacteroidetes’ (Garrity & Holt, 2001). The closest relative of strain WB4T found in GenBank was an uncultured bacterial clone (118ds10) from downstream of a collapsed equine manure pile, with a 16S rRNA gene sequence similarity of 99·7 % (Simpson et al., 2004). The second (similarity of 97·2 %) to fifth closest (95·1 %) relatives were all environmental clones (Moissl et al., 2002; Harris et al., 2004), with which strain WB4T formed a distinct cluster (Fig. 2). The closest recognized species to strain WB4T were Dysgonomonas capnocytophagoides (formerly CDC group DF-3) CCUG 17996T (Hofstad et al., 2000) (90·9 %), Dysgonomonas mossii CCUG 43457T (Lawson et al., 2002) (89·8 %) and Bacteroides merdae ATCC 43184T (88·7 %). Tannerella forsythensis (formerly Bacteroides forsythus) ATCC 43047T (Sakamoto et al., 2002) and Bacteroides fragilis ATCC 25285T (Holdeman et al., 1984) were the next most closely related species, with sequence similarities of 87·4 and 86·6 %, respectively (Fig. 2).
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. Cells of these species are commonly Gram-negative, non-motile and non-spore-forming rods. D. capnocytophagoides and D. mossii are facultative anaerobes isolated from human clinical specimens and grow well aerobically and anaerobically at 35–37 °C (Hofstad et al., 2000; Lawson et al., 2002). B. merdae is a strict anaerobe isolated from human faeces and has an optimum growth temperature of 37 °C (Johnson et al., 1986). The other two related species discussed above are derived from deep periodontal pockets of humans (T. forsythensis) (Sakamoto et al., 2002) or various types of human clinical specimens (B. fragilis) (Holdeman et al., 1984). Both are strict anaerobes and have optimum growth temperatures of about 37 °C. Thus, species related to strain WB4T are mainly isolates from humans and other warm-blooded animals (Paster et al., 1994).
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; Johnson et al., 1986; Hofstad et al., 2000; Lawson et al., 2002; Sakamoto et al., 2002), whereas strain WB4T was highly sensitive to bile salts.
Major end-products from glucose of D. capnocytophagoides are propionate, lactate and succinate (Hofstad et al., 2000) and those of B. merdae are succinate and acetate with a trace amount of propionate (Johnson et al., 1986) (Table 1
). Furthermore, T. forsythensis produces various acids such as acetate, butyrate, isovalerate, propionate, phenylacetate and succinate (Sakamoto et al., 2002) and B. fragilis usually produces acetate and succinate as major products with propionate as a minor product (Holdeman et al., 1984; Moore et al., 1994). Strain WB4T produced propionate and acetate at a ratio of 2 : 1 as the major products from glucose together with a smaller amount of succinate. Thus, although propionate and succinate seem to be common end-products for these related organisms, the physiological characteristics of their fermentative metabolism differ.
The G+C content of the genomic DNA of strain WB4T (39·3±1·0 mol%) was similar to those of D. capnocytophagoides (38 mol%) (Hofstad et al., 2000) and D. mossii (38·5 mol%) (Lawson et al., 2002), but was somewhat lower than that of B. merdae (44 mol%) (Johnson et al., 1986) (Table 1). It is also lower than those of T. forsythensis (44–48 mol%) (Sakamoto et al., 2002) and B. fragilis (41–44 mol%) (Holdeman et al., 1984). The respiratory quinones of B. merdae are MK-9 and MK-10 and those of T. forsythensis and Bacteroides species are commonly MK-10 and MK-11 (Sakamoto et al., 2002). Thus, strain WB4T has a distinctly different quinone composition from those of related species.
The CFA profiles of strain WB4T and related species are presented in Table 2. Anteiso-C15 : 0, iso-C15 : 0, iso-C17 : 0 3-OH and C16 : 0 are the major CFAs found in Bacteroides species (Miyagawa et al., 1979; Moore et al., 1994). The overall CFA profiles of B. merdae, T. forsythensis and B. fragilis are generally consistent with this, although some of these signature fatty acids are only minor components in B. merdae and T. forsythensis. D. capnocytophagoides also has anteiso-C15 : 0 as a dominant CFA (19·6 %), but its profile is rather different from the other three species in having iso-C14 : 0 (19·8 %) and iso-C16 : 0 3-OH (12·3 %) as predominant CFAs. Strain WB4T also has anteiso-C15 : 0 (30·8 %) as the predominant fatty acid, but its overall profile is significantly different from those of any related species. Fatty acids such as iso-C15 : 0, iso-C17 : 0 3-OH and C16 : 0 are relatively minor components in strain WB4T, whereas anteiso-C17 : 0 3-OH (17·9 %) and C15 : 0 (19·0 %) are major components. Anteiso-C17 : 0 3-OH is also present in B. merdae and T. forsythensis, but it is only a minor component, and it is not found in B. fragilis or D. capnocytophagoides. The predominance of C15 : 0 (19·0 %) in strain WB4T is also unique among the related species except for D. capnocytophagoides.
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). The second most closely related clone (similarity of 97·2 %) was isolated from a cold sulfidic marsh in Germany (Moissl et al., 2002) and the third closest (96·3 %) was isolated from a Gallionella community located on Boulder Creek, CO, USA (Harris et al., 2004). Other relatives with sequence similarities higher than about 95 % were all environmental clones, with which strain WB4T formed a distinct cluster (Fig. 2). These data suggest that an unknown bacterial linage closely related to strain WB4T might be widespread and numerous in natural environments. Based on the data presented, we propose here a novel genus, Paludibacter gen. nov., with Paludibacter propionicigenes sp. nov. as the type species.
Description of Paludibacter gen. nov.
Paludibacter (Pa.lu.di.bac'ter. L. n. palus -udis a swamp, marsh; N.L. masc. n. bacter a rod; N.L. masc. n. Paludibacter rod living in swamps).
Cells are Gram-negative, non-spore-forming, non-motile, short rods. Strictly anaerobic. Chemo-organotroph. Optimum growth temperature is 30 °C. Oxidase, catalase and nitrate-reducing activities are negative. Species utilize various sugars and produce acetate and propionate as major fermentation end-products with succinate as a minor product. Major cellular fatty acids are anteiso-C15 : 0, C15 : 0 and anteiso-C17 : 0 3-OH. The major respiratory quinone is MK-8(H4). The genomic DNA G+C content of the type species is 39·3 mol%. The type species is Paludibacter propionicigenes.
Description of Paludibacter propionicigenes sp. nov.
Paludibacter propionicigenes (pro.pi.on.i.ci'ge.nes. N.L. n. acidum propionicum propionic acid; Gr. v. gennao to produce; N.L. part. adj. propionicigenes propionic acid-producing).
Has the following properties in addition to those given for the genus. Cells are 0·5–0·6 µm in diameter and 1·3–1·7 µm in length. Ends of cells are usually round to slightly tapered and elongated cells are occasionally formed both singly and in chains of the short cells. Spherical cells sometimes develop after storage of slant cultures at 4 °C. Propionate and acetate are produced as major fermentation products from glucose at a ratio of 2 : 1. Grows at pH 5·0–7·6 (optimum pH 6·6) and at 15–35 °C. Even at 33 °C, growth is significantly slower than that at 30 °C. Does not grow at 37 °C. NaCl concentration range for growth is 0–0·5 % (w/v) in PYG medium. Utilizes arabinose, xylose, cellobiose, fructose, galactose, glucose, mannose, maltose, melibiose, glycogen and soluble starch as growth substrates and produces acids. Does not use ribose, sorbose, lactose, rhamnose, sucrose, trehalose, melezitose, raffinose, cellulose, xylan, salicin, dulcitol, inositol, mannitol, sorbitol, ethanol, glycerol, fumarate, lactate, malate, pyruvate 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 type strain, WB4T (=JCM 13257T=DSM 17365T), was isolated from rice plant residue in anoxic rice-field soil in Japan.
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ACKNOWLEDGEMENTS |
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M. Sakamoto and Y. Benno Reclassification of Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae comb. nov. Int J Syst Evol Microbiol, July 1, 2006; 56(Pt 7): 1599 - 1605. [Abstract] [Full Text] [PDF]
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