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1 Faculty of Agriculture, Yamagata University, Wakaba-machi 1-23, Tsuruoka 997-8555, Japan
2 Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 6, Higashi 1-1-1, Tsukuba 305-8566, Japan
Correspondence
Atsuko Ueki
uatsuko{at}tds1.tr.yamagata-u.ac.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 13 June 2003 as DOI 10.1099/ijs.0.02764-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains WdT and Wf are AB078858 and AB078859, respectively.
Micrographs of strains WdT and Wf are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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) become anoxic after flooding and the methanogenic microbial community develops with active degradation of organic matter (Takai, 1970; Seiler et al., 1984; Glissmann & Conrad, 2000). Thus, the rice-field ecosystem is considered to be one of the major sources of global atmospheric methane (Khalil, 2000). Many studies have investigated anaerobic microbial communities in anoxic rice-field soil (Janssen et al., 1997; Großkopf et al., 1998; Henckel et al., 1999; Hengstmann et al., 1999) and novel anaerobic micro-organisms have been isolated (Rajagopal et al., 1988; Asakawa et al., 1995; Chin et al., 1998, 1999; Rosencrantz et al., 1999; Wind et al., 1999; Satoh et al., 2002).
Japan is located in the rice-producing district of Asia and rice cultivation using irrigated fields has been practiced for a long time. Rice straw and remaining plant residue, such as rice stubble and roots, are ploughed into the soil at the beginning of the growing season to act as organic fertilizers. Such additions often result in an increase in methane emission rates from the fields (Yagi & Minami, 1990; Watanabe et al., 1995; Wassman et al., 2000a). In a previous study, we reported the enumeration and isolation of anaerobic fermentative bacteria from rice-plant residue ploughed into the soil of a Japanese rice field (Akasaka et al., 2003). Of the 47 bacterial isolates that were analysed by means of 16S rDNA sequence, five strains in the Actinobacteria commonly produced propionate from glucose. This group was phylogenetically distinct and was tentatively named the ‘propionate-producing Actinobacteria group’. We have investigated the phenotypic characteristics of representative strains of this group and from the results obtained, we propose a novel genus and species, Propionicimonas paludicola gen. nov., sp. nov., for these isolates.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Rice straw had been applied annually to this plot for more than 20 years. Cultivation practices for rice plants and characteristics of the soil were described previously (Ueki et al., 1999, 2000; Kaku et al., 2000; Hattori et al., 2001, 2002). Strains were isolated by selecting individual colonies after counting anaerobic bacteria on plant residue collected from the soil. Methods used have been described previously (Hungate, 1966; Holdeman et al., 1977; Akasaka et al., 2003). Strains W1, WdT and Wf were isolated from rice-straw samples, whereas strains K2 and K5 were derived from rice stubble and roots. Strains W1, K2 and K5 were isolated in May, during the flooding period of the field, and the other strains were isolated in August, during the intermittent irrigation period (Akasaka et al., 2003).
Culture conditions.
Strains were cultivated anaerobically at 30 °C by using peptone/yeast extract (PY) medium as basal medium with oxygen-free, 95 % N2/ 5 % CO2 mixed gas as the headspace, as described previously (Akasaka et al., 2003). PY medium supplemented with (l-1) 0·25 g each of glucose, cellobiose, maltose and soluble starch, as well as 50 ml plant residue extract (RE) and 15 g agar (Difco), was designated PY4SR agar and used for maintenance of the strains in agar slants. Plant residue collected from the RS plot during the flooding period was autoclaved (120 °C for 30 min) with a fivefold amount (wet-weight basis) of deionized H2O and the supernatant obtained after centrifugation was used as RE for the provision of growth factors. PY liquid medium supplemented with 10 g glucose l-1 (PYG medium) was usually used for cultivation of the cells. For PY liquid medium, cyanocobalamin (cobalamin) (vitamin B12; Kanto Chemical) was added at 50 µg l-1 as a growth factor as described below, unless stated otherwise. Media were adjusted to pH 7·3 with 1 M NaOH. For estimation of optimal growth conditions, strains were cultivated at different temperatures (10–50 °C), pH values (4·6–7·5 in PYG medium) and NaCl concentrations (0–5·0 % in PYG medium). Growth in liquid medium was monitored by changes in OD660.
Morphological characteristics.
Morphology of cells was observed by Gram-staining, phase-contrast microscopy and transmission electron microscopy (TEM). For TEM, a centrifuged cell pellet was fixed with 5 % (v/v) glutaraldehyde and 1 % (v/v) osmium tetroxide. Ultrathin sections of the sample, embedded in epoxy resin (Kushida, 1980), were prepared with a Reichert ultramicrotome. Samples were stained with uranyl acetate and lead citrate and examined with a Hitachi H-7000 transmission electron microscope.
Physiological and biochemical characterization.
Growth of strains under aerobic conditions was examined by plate culture on nutrient agar (Nissui Pharmacy) and PY4SR agar. Spore formation was assessed after Gram-staining, as well as under phase-contrast microscopy and by subsequent growth in PYG medium of cells exposed to 80 °C for 10 min. Oxidase, catalase and nitrate-reducing activities were determined according to methods described previously (Satoh et al., 2002; Akasaka et al., 2003). Utilization of carbon sources was tested in PY liquid medium with each substrate added at 10 g l-1 (for mono-, di-, tri- and polysaccharides and sugar alcohols) or 30 mM (for alcohols and organic acids). Fermentation products were analysed as described previously (Ueki et al., 1986; Akasaka et al., 2003). Glucose concentrations in the media were measured with a D-glucose kit (Boehringer Mannheim) according to the manufacturer's protocol. All phenotypic characterizations, including the following chemotaxonomic analyses, were carried out in duplicate.
Quinone, fatty acid and cell-wall analyses.
Quinones were extracted from freeze-dried cells with chloroform/methanol (2 : 1, v/v) and n-hexane. Extracts were purified by using Sep-Pak Plus (Waters) and analysed by reverse-phase HPLC for identification (Tamaoka et al., 1983). Whole-cell fatty acids were converted to methyl esters by treatment with anhydrous methanolic HCl (Ueki & Suto, 1979; Komagata & Suzuki, 1987). Methyl esters were extracted with n-hexane and analysed by using a GC-mass spectrometer (M7200A GC/3DQMS; Hitachi) equipped with a DB-5ms capillary column coated with 5 % phenylmethylpolysiloxane at a thickness of 250 nm (Hanada et al., 2002). The presence of diaminopimelic acid (DAP) isomers in the cell-wall peptidoglycan was determined by TLC (no. 5716; Merck) after hydrolysis with 6 M HCl at 100 °C for 18 h (Komagata & Suzuki, 1987).
DNA base composition.
Genomic DNA was extracted according to a method described previously (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 (model LC-6A system; Shimadzu) equipped with a CLC-ODS column (6x150 mm; Shimadzu).
16S rDNA sequence and phylogenetic analysis.
16S rDNA of strains was extracted according to a method described previously (Akasaka et al., 2003) and amplified by PCR. PCR-amplified 16S rDNA was sequenced by using a Thermo Sequenase Primer Cycle Sequencing kit (Amersham Biosciences) and a model 4000L DNA sequencer (LI-COR). Multiple alignments of isolates' 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 assemblages.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). However, the five isolates could be divided into two groups according to their growth in PYG medium. Four isolates (W1, WdT, K2 and K5) showed extremely slow growth rates without addition of any growth factors, whereas strain Wf grew well. For slow-growing isolates, 16S rDNA similarities among three strains (W1, WdT and K5) were 99·4–99·7 %, whereas those with strain K2 were lower (98·0–98·3 %).
By screening possible growth factors, addition of cobalamin to PYG medium markedly stimulated the growth of the four slow-growing strains. Table 1 shows the effects of cobalamin addition on growth (final OD660) and fermentation end products. In PYG medium without added cobalamin, all isolates except strain Wf formed small amounts of products, with lactate as the predominant one. In the presence of added cobalamin, production of propionate was stimulated together with acetate, whilst lactate changed to a minor product. Although strain Wf produced large amounts of fatty acids in PYG medium with no growth factor addition, cobalamin also stimulated its growth and production of propionate, again with a concomitant suppression of lactate production. All isolates produced CO2 as well as fatty acids, but hydrogen production was not observed.
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Strains WdT and Wf were selected and characterized in more detail. In later experiments, both isolates were cultured in media that contained an excess amount of cobalamin (50 µg l-1).
Colony and cell morphologies
Strains WdT and Wf grew anaerobically on PY4SR agar and produced white colonies of 2–3 mm diameter after 2–3 days incubation. Cells were Gram-positive, pleomorphic, often slightly curved rods, 0·4–0·5 µm in diameter and 1·4–2·2 µm in length. Irregular V- or crescent-shaped cell arrangements were observed frequently (see Supplementary Figs a and c, available as supplementary material in IJSEM Online). Cells were non-motile under phase-contrast microscopy. TEM showed that cells had a cell-wall structure typical of Gram-positive bacteria (Supplementary Figs b and d). Electron-translucent regions in the cells revealed the presence of intracellular storage compounds. Spore formation was not observed and cells treated at 80 °C for 10 min did not grow.
Physiological and biochemical characteristics
Strains WdT and Wf had very similar physiological and biochemical characteristics. Both grew weakly in air on both PY4SR and nutrient agar, but much better growth was observed under anaerobic conditions. Both utilized arabinose, xylose, fructose, galactose, glucose, mannose, cellobiose, maltose, sucrose, trehalose, glycerol and mannitol as carbon sources, whereas utilization of ribose and lactose was poor. Both strains grew on pyruvate and lactate; very weak growth was observed with malate, fumarate and succinate. Neither strain utilized fucose, rhamnose, sorbose, melibiose, melezitose, raffinose, cellulose, glycogen, soluble starch, xylan, adonitol, dulcitol, erythritol, inositol, sorbitol, ethanol, methanol or propanol as growth substrates. Other physiological characteristics of the two isolates are shown in Table 2.
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Phylogenetic analysis based on 16S rDNA sequences
A phylogenetic tree based on 16S rDNA sequences was constructed (Fig. 1). Sequence similarity between the 16S rDNA of strains WdT and Wf was 99·1 %; both strains formed a cluster close to the genera Micropruina (Shintani et al., 2000), Microlunatus (Nakamura et al., 1995) and Friedmanniella (Schumann et al., 1997) in the Actinobacteria. The closest relative of both strains was Micropruina glycogenica (Shintani et al., 2000), with sequence similarities of 95·8 and 95·7 %, respectively. The closest relative to strain WdT found in GenBank was environmental clone SJA-181 (Fig. 1), which was derived from an anaerobic microbial consortium in a trichlorobenzene-transforming bioreactor (von Wintzingerode et al., 1999), with 16S rDNA sequence similarity of 98·3 %.
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Propionate is an important intermediate in methanogenic decomposition of organic matter in anoxic rice-field soils (Dolfing, 1988; Glissmann & Conrad, 2000; Chin et al., 2001; Chin & Janssen, 2002). The striking effects of cobalamin on growth and fermentation of the isolates suggest that survival of the group on plant residue at a rather high population density depends on the availability of cobalamin from the environment. A similar requirement for cobalamin has been reported in a ruminal propionate-producing bacterium, Prevotella ruminicola (Strobel, 1992).
Many propionate-producing bacteria produce propionate through conversion of succinyl-CoA to methylmalonyl-CoA, which is catalysed by a vitamin B12-dependent methylmalonyl-CoA isomerase (Roth et al., 1996). Stimulation of propionate production by added cobalamin suggests that this pathway is present in the isolates described here. Many other anaerobes, including methanogens and acetogens, synthesize cobalamin endogenously for their own use and several reactions, including reductive dehalogenation of chlorinated compounds, depend on cobalamin or vitamin B12 (Krone et al., 1989; Stupperich et al., 1990; White & Zhou, 1993; Roth et al., 1996). Thus, cobalamin synthesized by various microbial groups may be released into the environment, where it may support the growth of cobalamin-requiring bacteria.
Phenotypic and phylogenetic characteristics of strains WdT and Wf were almost the same, except for a requirement for cobalamin for their optimal growth. Micropruina glycogenica was the most closely related known species to both isolates, based on 16S rDNA sequence as described above, followed by Microlunatus phosphovorus (Nakamura et al., 1995) (similarity of 94·7–95·8 %) and Friedmanniella antarctica (Schumann et al., 1997) (similarity of 93·1 %), all in the family Propionibacteriaceae within the Actinobacteria (Garrity & Holt, 2001) (Fig. 1). These data agree with the base compositions of their genomic DNA, which indicate that they both belong to the high-G+C Gram-positive bacteria. However, many differences exist between the characteristics of these isolates and those of other closely related species (Table 2).
Their cellular morphologies show that the isolates are irregular rods, whereas other related species have spherical cells. The isolates are facultatively anaerobic and catalase-negative and grow well under anoxic conditions, whereas the other three species are strictly aerobic and catalase-positive. Both Micropruina glycogenica and Microlunatus phosphovorus have oxidase and nitrate-reducing activities, but the novel isolates do not. Furthermore, their cellular fatty acid composition profiles are different from those of their close relatives: major fatty acids of the isolates are C13 : 0, anteiso-C15 : 0 and C15 : 0, whereas those of the other three are iso-C14 : 0, iso-C15 : 0, anteiso-C15 : 0, iso-C16 : 0 or C16 : 0. Fatty acids C13 : 0 and C15 : 0 are absent from, or only minor components in, other related species. Furthermore, most predominant fatty acids in their relatives, except for anteiso-C15 : 0, are absent from, or only minor components in, the isolates described here. In addition to MK-9(H4), both isolates contain MK-10(H4) as a predominant menaquinone, whereas the other three species do not (Nakamura et al., 1995; Schumann et al., 1997; Maszenan et al., 1999; Shintani et al., 2000). Among their close relatives, only Micropruina glycogenica has meso-DAP in the peptidoglycan of the cell wall (Shintani et al., 2000).
The isolates produce propionate in the presence of excess cobalamin and their fermentation patterns resemble those of Propionibacterium spp. (Cummins & Johnson, 1986) and Propioniferax spp. (Yokota et al., 1994; Pitcher & Collins, 1991) in the family Propionibacteriaceae (Garrity & Holt, 2001). Despite this, they are only distantly related to Propionibacterium propionicum and Propioniferax innocua, based on 16S rDNA sequence data (similarities of 91·5–92·0 and 90·0 %, respectively) (Fig. 1). Furthermore, both Propionibacterium propionicum and Propioniferax innocua contain LL-DAP in their cell-wall peptidoglycan and MK-9(H4) as the sole menaquinone (Maszenan et al., 1999). The predominant cellular fatty acids in Propioniferax innocua are also iso-C15 : 0 and anteiso-C15 : 0 (Schumann et al., 1997).
On the basis of both the phylogenetic and phenotypic characteristics described above, we conclude that WdT and Wf should be assigned to the same species within a novel genus, Propionicimonas gen. nov., with Propionicimonas paludicola sp. nov. as the type species.
Description of Propionicimonas gen. nov.
Propionicimonas (Pro.pi.on.i.ci.mo'nas. N.L. n. acidum propionicum propionic acid; Gr. fem. n. monas a unit, monad; N.L. fem. n. Propionicimonas propionic acid-producing monad).
Cells are Gram-positive, irregular rods. Facultatively anaerobic chemo-organotroph. Non-motile and non-spore-forming. Mesophilic. Oxidase-, catalase- and nitrate reduction-negative. Propionate is produced anaerobically from glucose. Cell-wall peptidoglycan contains meso-DAP; major cellular fatty acids are C13 : 0, anteiso-C15 : 0 and C15 : 0. MK-9(H4) and MK-10(H4) are the major quinones. Genomic DNA G+C content is 68·7 mol%. On the basis of 16S rDNA sequences, the bacterium belongs to the class Actinobacteria. The genera Micropruina, Microlunatus and Friedmanniella are related most closely to this genus. The type species is Propionicimonas paludicola.
Description of Propionicimonas paludicola sp. nov.
Propionicimonas paludicola (pa.lu.di'co.la. L. n. palus, -udis swamp, marsh; L. suff. -cola derived from incola inhabitant, dweller; N.L. masc. n. paludicola an inhabitant of swamps).
Gram-positive, irregular, often slightly curved rods, 0·4–0·5 µm in diameter and 1·8–2·0 µm in length and frequently arranged in irregular V- or crescent-shapes. Optimal growth occurs at 35 °C and pH 6·5. Grows in the presence of up to 2·0 % (w/v) NaCl. Cells produce acetate, propionate, lactate, succinate and CO2 anaerobically from glucose. Growth and production of propionate are both stimulated by addition of cyanocobalamin to the medium. Cells grow on arabinose, xylose, fructose, galactose, glucose, mannose, cellobiose, maltose, sucrose, trehalose, glycerol, mannitol, pyruvate and lactate, but growth is scarce on ribose, lactose, malate, fumarate and succinate. Fucose, rhamnose, sorbose, melibiose, melezitose, raffinose, cellulose, glycogen, soluble starch, xylan, adonitol, dulcitol, erythritol, inositol, sorbitol, ethanol, methanol and propanol are not utilized. Chemotaxonomic characteristics of the species are the same as those described for the genus.
The type strain is WdT (=JCM 11933T=DSM 15597T). Isolated from rice-plant residue ploughed into the soil of a Japanese rice field.
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ACKNOWLEDGEMENTS |
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-Proteobacteria (Garrity & Holt, 2001