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Department of Life Sciences, National Chung Hsing University, Taichung, Taiwan, ROC
Correspondence
Mei-Chin Lai
mclai{at}dragon.nchu.edu.tw
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ABSTRACT |
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 TOP ABSTRACT MAIN TEXTREFERENCES |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain ML15T is AY186542.
An EM of strain ML15T and graphs showing the effects of temperature, pH and salinity on growth of strain ML15T are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Blotevogel et al., 1991; Boone et al., 1993; Corder et al., 1983; Jain et al., 1988; Lai & Chen, 2001; Maestrojuán et al., 1990; Ollivier et al., 1986, 1998; Rivard & Smith, 1982; Romesser et al., 1979; Rouvière et al., 1992; Widdel, 1986; Widdel et al., 1988; Xun et al., 1989; Zellner et al., 1997, 1998, 1999).
The genus Methanofollis, which includes Methanofollis tationis Chile 9T and Methanofollis liminatans strains GKZPZT and BM1, was formally proposed by Zellner et al. (1999) on the basis of 16S rRNA gene sequencing and chemotaxonomic and physiological data. Methanofollis tationis Chile 9T was isolated from a solfataric field on Mount Tatio in the Atacama Desert in northern Chile (Zabel et al., 1984), whereas Methanofollis liminatans GKZPZT and BM1 were isolated from an industrial wastewater reactor in Germany (Zellner et al., 1990, 1999). Recently, a novel methanogen isolated from an aquaculture fish pond near Wang-gong, Taiwan, was reported as Methanofollis aquaemaris N2F9704T (Lai & Chen, 2001). These three Methanofollis species are all mesophilic, highly irregular cocci that use H2/CO2 and formate for growth and methanogenesis. However, Methanofollis aquaemaris N2F9704T differs from the other strains in its source, substrate utilization, Mr of the S-layer protein subunit, effect of tungsten on growth and optimal ranges of NaCl and pH for growth. Moreover, the 16S rRNA gene sequence similarities of Methanofollis aquaemaris N2F9704T with the other Methanofollis species were 94·7–95·5 % (Lai & Chen, 2001). In this report, the isolation and characterization of a novel methanogen, strain ML15T, which was isolated from an aquaculture fish pond in Taiwan, are described; it is proposed that this strain represents a novel species, Methanofollis formosanus sp. nov.
Strain ML15T was isolated from a water sample of a marine aquaculture fish pond near Wang-gong, Taiwan, the same sampling site used for isolation of Methanofollis aquaemaris N2F9704T (Lai & Chen, 2001). Sea water and ground water were mixed and pumped into a man-made pond to obtain 10–20 
practical salinity units for the mixed cultivation of Chanos chanos (white mullet) and Meretrix lusoria (Lai et al., 1999). Sampling, enrichment and isolation methods for strain ML15T were according to Lai & Chen (2001). The modified anaerobic technique of Hungate was performed (Balch et al., 1979; Sowers & Noll, 1995) and sterilized media were prepared under an oxygen-free N2 : CO2 (4 : 1) atmosphere. The composition and preparation of MB medium was as described previously (Lai & Chen, 2001). MB/W medium was MB medium with tungstate (Na2WO4, 0·3 mg l–1). Minimal medium (MM) was MB medium without the addition of yeast extract and tryptone.
Enrichment was begun immediately after the sample was brought to the laboratory. Strain ML15T was isolated and purified as described previously (Lai & Chen, 2001; Lai et al., 2002, 2004). Samples (5 ml) from sediments of the marine water aquaculture fish pond were inoculated into a bottle of MB medium (45 ml) containing methanol as methanogenic substrate. The production of methane was determined by GC with flame-ionization detection (Lai et al., 1999). After 1 month incubation at room temperature, methanogenesis occurred and, after four successive transfers, the methanogenic culture was then inoculated into roll-tube MB/W agar medium for further isolation. Under the fluorescent microscope, a fluorescence-positive colony with a small opaque centre and irregular translucent margin was picked and transferred to 5 ml MB/W medium with methanol in the Coy anaerobic chamber. The culture grew poorly, but good growth was observed after it was further transferred to MB/W medium with formate as substrate. Methane-producing cultures from this single colony were further purified by combining the serial dilution method (10–4), antibiotic tetracycline (100 µg ml–1) and roll tube method until contamination by non-methanogens was not detectable. This isolate, strain ML15T, was previously known as N2M9705.
Cells of strain ML15T were non-motile, irregular cocci, 1·5–2·0 µm in diameter and stained Gram-negative. Under the phase-contrast microscope (Olympus BH-2), the irregular coccus cells appeared with a dark centre surrounded by a transparent outer layer. Refractive areas were observed in the cells. As observed by SEM ABT-150S (sample preparation as described by Lai et al., 1999), strain ML15T presented irregular flat, disc-shaped cells with concavity (Fig. 1) and planes of division were frequently detected. Cells lysed rapidly in the presence of SDS (0·1 g l–1), indicating that the cell envelope consisted of a protein surface layer (Boone & Whitman, 1988). The proteinaceous cell wall structure of strain ML15T was very sensitive to physical forces, such as those exerted by centrifugation and pipetting, and lysed easily. Negative staining of strain ML15T was performed as described previously (Lai & Shih, 2001) and cells observed under TEM (JEM-200cx; JEOL) showed a hexagonally arranged pattern of S-layer protein (see Supplementary Fig. A available in IJSEM Online). The centre-to-centre spacing of the morphological units of the S-layer lattice of strain ML15T was about 16·4 nm. Surface-layer proteins were isolated according to the protocol of König (1995). SDS-PAGE was performed as described by Laemmli (1970) and Coomassie blue R-250 was used to visualize protein. Analysis of the S-layer indicated it was composed of a protein subunit with an Mr of 138 800.
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The optimal growth parameters of strain ML15T were tested using cells grown in MB/W medium with formate plus acetate. Strain ML15T could grow at 25–42 °C and optimal growth was observed at 40 °C. Temperatures below 20 °C or above 50 °C completely inhibited growth of cells (Supplementary Fig. B). Strain ML15T grew at pH 5·6–7·3, with optimal growth at pH 6·6–7·0 (Supplementary Fig. B). At pH values greater than 7·7, cell growth was completely inhibited suggesting that cells are sensitive to an alkaline environment. Cells of strain ML15T could tolerate NaCl concentrations of 0–4 %, but not above 6 %. The optimal NaCl concentration for growth of strain ML15T was 3 %, with a doubling time of 20 h (Supplementary Fig. B).
The sensitivity of strain ML15T to ampicillin, penicillin G, spectinomycin, kanamycin, tetracycline and chloramphenicol (each at a concentration of 100 µg ml–1) was tested in MB/W medium with sodium formate (100 mM) plus acetate (20 mM) and 0·5 % NaCl at 37 °C. Results indicated that strain ML15T was resistant to ampicillin, penicillin, kanamycin and spectinomycin and sensitive to chloramphenicol; tetracycline inhibited cell growth.
The melting temperatures of DNA from Methanofollis aquaemaris N2F9704T and strain ML15T were obtained as described previously (Jan et al., 1999; Lai et al., 2004; Marmur & Doty, 1962) and were 93·52 and 93·25 °C, respectively. The DNA G+C contents of Methanofollis aquaemaris N2F9704T and strain ML15T were 59·07 and 58·41 mol%, respectively.
For phylogenetic analysis, DNA was isolated by the general procedure of Jarrell et al. (1992). Approximately 30 ng DNA was used as a template for PCR amplification of an approximately 1300 bp portion of the 16S rRNA gene. PCR amplification primers used were forward primer coccus 1 (5'-CGACTAAGCCATGCGAGTC-3') and reverse primer reverse 3 (5'-GTGACGGGCGGTGTGTGCAAG-3'). The sequences were checked by the program CHECK-PROBE from the Ribosomal Database Project (Maidak et al., 1996) and corresponded to positions 23–41 and 1327–1309 in the 16S rRNA nucleotide sequence of Methanofollis aquaemaris N2F9704T (AF262035). As well as the two amplification primers, two additional primers were used for sequencing: shih2 (5'-CGATTACAGGGTTTCACTCCTACC-3') and primer follis1 (5'-TAATCGGTACGGGTTGTG-3') (Methanofollis aquaemaris N2F9704T, accession number AF262035, sequence positions 506–482 and 124–141, respectively). The resulting sequence of strain ML15T was assembled to produce an approximately 1287 base contiguous rRNA gene sequence (positions 22–1308). Gene sequences of the archaea used were obtained from the Ribosomal Database Project and GenBank. The similarity matrix was obtained based on the analytical results of the Ribosomal Database Project (http://rdp.cme.msu.edu/html/). Multiple sequence alignments were analysed using the package CLUSTAL_W at the Biology Workbench (http://workbench.sdsc.edu/). Distances were computed with the package CLUSTAL TREE at the same website using the neighbour-joining model and fed to DRAWGRAM in the program package PHYLIP version 3.5c (Felsenstein, 1993). Bootstrap confidence analysis was performed with SEQBOOT of the PHYLIP package using 1000 replicates.
The 16S rRNA gene sequence (1287 nt) of strain ML15T was determined and phylogenetic trees were constructed using a selection of sequences from related methanogens obtained from the GenBank database (Fig. 2). 16S rRNA gene sequence similarities between strain ML15T and other members of the families Methanocorpusculaceae, Methanomicrobiaceae and Methanoplanaceae were 85, 91–96 and 91 %, respectively. 16S rRNA gene sequence analysis placed strain ML15T close to Methanofollis aquaemaris N2F9704T (sequence similarity 97·2 %), Methanofollis liminatans GKZPZT (95·5 %) and Methanofollis tationis Chile 9T (96·3 %).
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). Devereux et al. (1996) and Fry et al. (1991) have proposed that a similarity of less than 98 % in a 16S rRNA sequence is evidence for separate species. The closest relative to strain ML15T was Methanofollis aquaemaris strain N2F9704T at 97·2 % similarity; Methanofollis liminatans GKZPZT (sequence similarity 95·5 %) and Methanofollis tationis Chile 9T (sequence similarity 96·3 %) were also closely related. The 16S rRNA gene sequence similarity of strain ML15T to the other members of the Methanomicrobiales was 85–93 %. Characteristics that differentiate strain ML15T from related Methanofollis species are listed in Table 1. These phylogenetic, phenotypic and physiological distinctions indicate that strain ML15T represents a novel Methanofollis species, for which the name Methanofollis formosanus sp. nov. is proposed.
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) and Methanofollis aquaemaris strain N2F9704T (Lai & Chen, 2001). All these organisms are mesophilic, highly irregularly cocci that use H2/CO2 and formate for growth and methanogenesis. Although strain ML15T shares these traits with Methanofollis species, it differs from these species in its source, mobility, substrate utilization and requirements, halotolerance, alkali tolerance, Mr of S-layer protein subunits, growth in the presence of tungsten and phylogenetics (Table 1
). Strain ML15T and Methanofollis aquaemaris strain N2F9704T were isolated from the same source (aquaculture fish pond) and, morphologically, they are very similar, non-motile irregular cocci, unlike Methanofollis tationis and Methanofollis liminatans, which were motile with flagella. Cells of members of the family Methanomicrobiaceae have hexagonal S-layer lattices consisting of glycoprotein subunits with Mr of 101 000–155 000 (Zellner et al., 1999). All Methanofollis species possess surface layer proteins as a cell envelope, forming a soft bag for the cells. The Mr of the S-layer protein subunits from ML15T and Methanofollis aquaemaris strain N2F9704T were 138 800 and 137 000, respectively; Mr of the S-layer protein subunits for Methanofollis tationis and Methanofollis liminatans were around 120 000. Also, both strain ML15T and Methanofollis aquaemaris strain N2F9704T could only use formate and H2/CO2 as catabolic substrates, could not utilize 2-propanol/CO2 or 2-butanol/CO2 and did not require acetate for cell growth, although it could reduce the lag time. In contrast, both Methanofollis tationis and Methanofollis liminatans required acetate for cell growth and M. liminatans could use 2-propanol/CO2 and 2-butanol/CO2 to produce methane.
Within the order Methanomicrobiales, the growth requirement for tungsten has been reported in Methanoculleus palmolei (Zellner et al., 1998) and Methanofollis tationis (Zabel et al., 1984). No growth was observed in Methanofollis tationis, an organism isolated from a solfataric field, if tungsten was not present in the growth medium (Zabel et al., 1984). In contrast, growth of the related organisms Methanofollis liminatans, isolated from effluent of a wastewater reactor (Zellner et al., 1990, 1999), Methanocalculus chunghsingensis, from an estuarine environment (Lai et al., 2002), and Methanofollis aquaemaris and strain ML15T, from an aquaculture fish pond (Lai et al., 2004 and this study), was greatly stimulated by tungsten, but the element was not absolutely required for growth. In the case of the estuarine isolate Methanocalculus taiwanensis P2F9704aT, the trace element tungsten was not required, but it slightly stimulated growth and could extend the growth range relating to temperature, pH and salt concentration (Lai & Chen, 2001).
All known Methanofollis species are mesophilic and neutrophilic. However, the pH range for growth of strain ML15T was pH 5·6–7·3 and cell growth was completely inhibited at pH 7·7, indicating that this strain is more sensitive to an alkaline environment than other species. Also, the optimal salt (NaCl) concentration for growth of strain ML15T was 3 %, which is the highest concentration observed in Methanofollis species. Phylogenetic (Fig. 2), phenotypic and physiological distinctions (Table 1) between Methanofollis species suggest that these species form two clusters, with M. aquaemaris and strain ML15T constituting one cluster. The 16S rRNA gene sequence similarities of Methanofollis aquaemaris and strain ML15T to Methanofollis liminatans GKZPZT were within the range 95·3–96·3 %.
Description of Methanofollis formosanus sp. nov.
Methanofollis formosanus (for.mo.sa'nus. N.L. masc. adj. formosanus from Formosa, the beautiful island of Taiwan).
Irregularly coccoid cells, non-motile, 1·5–2·0 µm in diameter. Obligately anaerobic cells. Stains Gram-negative. Cell wall has an SDS-sensitive S-layer protein with an Mr of 138 800. Catabolic substrates used include H2/CO2 and formate, but not acetate, methanol, trimethylamine, dimethylamine, ethanol, 2-propanol, iso-butanol, 2-butanol or dimethylamine. Cells are mesophilic and grow at 20–42 °C, with optimal growth at 37 °C. Cells grow at pH 5·6–7·3, with optimal growth at pH 6·6. Cells grow well in 0–4 % NaCl, with optimal growth at 3 % NaCl. Addition of acetate reduces the lag time and the trace element tungsten greatly promotes cell growth and extends the growth range. No growth is detected in minimal medium. Growth is completely inhibited by chloramphenicol and partly inhibited by tetracycline, but not by ampicillin, penicillin, kanamycin or spectinomycin. The G+C content of DNA of strain ML15T is 58·4 mol%.
The type strain is strain ML15T (=OCM 789T=DSM 15483T), isolated from a marine water aquaculture fish pond near Wang-gong, Taiwan.
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ACKNOWLEDGEMENTS |
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