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M. S. Swaminathan Research Foundation, 111 Cross St, Tharamani Institutional Area, Chennai, Madras 600 113, India
Correspondence
Sudha Nair
sudhanair{at}mssrf.res.in
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ABSTRACT |
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7c/9t/12t and 19 : 0cyclo 8c constituted 30·41 and 11·80 % total fatty acids, respectively, whereas 13 : 1 AT 12–13 was found at 0·53 %. DNA G+C content was 57·6–59·9 mol% and the major quinone was Q-10. Phylogenetic analysis based on 16S rRNA gene sequences showed that these strains were related to the genera Acidomonas, Asaia, Acetobacter, Gluconacetobacter, Gluconobacter and Kozakia in the Acetobacteraceae. Isolates were able to fix nitrogen and solubilized phosphate in the presence of NaCl. Based on overall analysis of the tests and comparison with the characteristics of members of the Acetobacteraceae, a novel genus and species is proposed for these isolates, Swaminathania salitolerans gen. nov., sp. nov. The type strain is PA51T (=LMG 21291T=MTCC 3852T).
The fatty acid composition of isolates and type strains is available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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), a novel species in a new genus within the family Acetobacteraceae, Swaminathania salitolerans gen. nov., sp. nov., is proposed.
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) supplemented with 250 mM NaCl. Vials were also inoculated with 100 µl serially diluted rhizosphere soil and non-rhizosphere soil suspensions. These were incubated at 30 °C for 5 days. Acid-producing and nitrogenase-positive vials with a yellow surface pellicle were streaked onto LGI agar plates and incubated at 30 °C. Pure cultures were obtained from individual colonies. In total, 41 strains were isolated and, after biochemical characterization, two isolates (PA12 and PA51T) were selected for further study.
The genomic DNA was extracted from isolates as described by Ausubel et al. (1987). A large fragment of the 16S rRNA gene was amplified using primers fD1 [5'-AGAGTTTGATCCTGGCTCAG-3'; positions 7–26 in Escherichia coli (Brosius et al., 1981)] and rP2 (5'-ACGGCTACCTTGTTACGACTT-3'; positions 1513–1494) as described previously (Weisburg et al., 1991; Loganathan, 2002). Amplification products were separated on a 1·5 % agarose gel in 1x TBE buffer. Products were purified using a Sephaglas BandPrep kit (Amersham Pharmacia Biotech) and the fragment was cloned using a Fermentas InsT/A clone PCR Product cloning kit according to the manufacturer's instructions. Clones were sequenced using the ABI PRISM Dye Terminator Ready Reaction kit (Applied Biosystems) according to the manufacturer's instructions. For sequencing, the following primers were used: M13 forward and reverse, PC513F (5'-CCCGGCTACTTCGTGC-3'; positions 513–518), PC513R (5'-GCACGAAGTAGCCGGG-3'; positions 518–513), PC970F (5'-CGCGCAGAACCTTACCAG-3'; positions 970–987) and PC970R (5'-CTGGTAAGGTTCTGCGCG-3'; positions 987–970). The BLAST algorithm (Altschul et al., 1997) was used to search nucleotide databases for similar sequences. Gene sequences were manually aligned with each other and multiple alignments of the sequences were carried out with the program CLUSTAL_W version 1.6 (Thompson et al., 1994). Distance matrices for the aligned sequences were determined using the two-parameter method of Kimura (1980). The neighbour-joining method was used to construct a phylogenetic tree (Saitou & Nei, 1987). The sequence data obtained were compared using 1450 bases. The robustness of individual branches was estimated by bootstrapping with 1000 replicates (Felsenstein, 1985).
A phylogenetic tree (Fig. 1) was constructed using 20 strains: including isolates PA12 and PA51T, and the type strains of Acetobacter aceti, Acidomonas methanolica, Asaia siamensis, Asaia bogorensis, Gluconacetobacter johannae, Gluconacetobacter azotocaptans, Gluconacetobacter diazotrophicus, Gluconacetobacter sacchari, Gluconacetobacter liquefaciens, Gluconacetobacter intermedius, Gluconacetobacter oboediens, Gluconacetobacter europaeus, Gluconacetobacter xylinus, Gluconobacter frateurii, Gluconobacter cerinus, Gluconobacter oxydans, Kozakia baliensis and Rhodospirillum rubrum. Isolates PA12 and PA51T constituted a separate branch within the lineage including species of the genus Asaia and distinct from the lineage containing species of the genera Acetobacter, Acidomonas, Gluconobacter, Gluconacetobacter and Kozakia. 16S rDNA sequences of isolates PA12 and PA51T were 99·9 % similar to each other. The sequence similarities of isolate PA51T with the type strains of Gluconobacter frateurii, Acidomonas methanolica, Acetobacter aceti, Gluconacetobacter xylinus, Gluconacetobacter johannae, Gluconacetobacter sacchari, K. baliensis and Asaia siamensis were 92·9, 93·2, 93·8, 94·1, 94·6, 95·1, 96·5 and 98·6 %, respectively.
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and Xu et al. (2000). DNA relatedness was assessed based on relative levels of reassociation to 32P-labelled total DNA, using the rediprime DNA-labelling kit (Amersham). Labelled DNA in independent experiments was from isolates and type strains. DNA–DNA reassociation was carried out for 16 h at 65 °C and the nylon filters were washed once in 1x SSC at room temperature for 15 min and once in 1x SSC for 5 min at 65 °C. Autoradiography was performed for 2 h, filter lanes were cut out and the radioactivity was estimated with a Beckman multi-purpose scintillation counter (LS 6500). The percentage reassociation was calculated for each strain tested in relation to the homologous control (Fuentes-Ramirez et al., 2001). Ubiquinone homologues were analysed quantitatively by HPLC with a C18 column. Standard preparations of Q-10 and Q-9 were prepared from cells of Gluconacetobacter diazotrophicus LMG 7603T and Acetobacter aceti LMG 1504T, respectively (Franke et al., 1999; Lisdiyanti et al., 2002).
Isolates PA12 and PA51T had a G+C content of 57·6–59·9 mol%, which was lower than that of the type strains of Asaia bogorensis and Asaia siamensis (59–61 mol%) and higher than that of K. baliensis (56–57 mol%) (Lisdiyanti et al., 2002). The isolates had high DNA–DNA similarity values (84–100 % between strains PA12 and PA51T) indicating that they belonged to the same species. Low similarity values (12–30 %) were observed with the type strains of Asaia bogorensis, Asaia siamensis and K. baliensis. The major quinone of the two isolates was Q-10.
The type of flagellation and the cell dimensions of strains PA12 and PA51T were determined using cells negatively stained with 2 % (v/v) aqueous uranyl acetate at pH 3·5 by TEM (model JEM 1200 EX11 JEO2). Five replications were used for each characterization in this study. Colony morphology was examined on LGI medium (Cavalcante & Dobereiner, 1988). Bacterial motility was tested by growth in semi-solid medium 0·3 % WL nutrient agar. Oxidase and catalase tests were determined using commercially available discs (Himedia). The production of water-soluble brown pigment was determined using GYC agar medium as described by Swings et al. (1992) and overoxidation of glucose and ethanol, lactate and acetate was conducted as described by De Ley et al. (1984) and Asai et al. (1964). Tolerance to NaCl was also tested in SM medium (De Ley & Swings, 1984). Pigmentation, growth on glutamate agar, ketogenic activity and acid production were tested using the methods of Asai et al. (1964).
Cellular fatty acid composition of strains PA12 and PA51T, and the type strains of Asaia bogorensis, Asaia siamensis and K. baliensis were estimated in cells grown on trypticase soy agar (without NaCl) for 48 h at 30 °C. Methyl esters of cellular fatty acids were prepared and identified following the instructions of the Microbial Identification system (MIDI; Hewlett Packard).
A summary of biochemical and physiological characteristics of strains PA12 and PA51T is presented in Table 2. Water-soluble brown pigment was produced on D-glucose- and CaCO3-containing agar plates. Catalase was positive and oxidase was negative. Brown pigmentation was observed on yeast extract-, D-glucose- and CaCO3-containing medium. The strains did not produce gelatinase. Acetate and lactate were oxidized to carbon dioxide and water, but the activity was weak. The isolates produced acetic acid from ethanol and grew in the presence of 0·35 % (v/v) acetic acid at pH 3·5 and 3 % NaCl using 1 % KNO3 as a nitrogen source. They also grew on mannitol and glutamate agar and did not utilize methanol as a sole source of carbon on Hoyer–Frateur medium. Acid was produced from L-arabinose, D-glucose, D-galactose, D-mannose, glycerol, sorbitol and ethanol, but not from L-rhamnose or D-mannitol.
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7c/9t/12t, which accounted for 30·41 % total fatty acid content in PA51T, compared with 43·76 % in Asaia bogorensis, 54·29 % in Asaia siamensis and 37·00 % in K. baliensis. Fatty acids common to these species included 14 : 0, 14 : 0 2-OH, 15 : 0, 16 : 0, 16 : 0 2-OH, 16 : 0 3-OH, 17 : 0, 18 : 0, 19 : 0cyclo 8c and 20 : 36,9,12c. However, strain PA51T contained 11·8 % 19 : 0cyclo 8c compared with <1 % in Asaia bogorensis and Asaia siamensis, and 5·6 % in K. baliensis. The fatty acid composition of isolates and type strains is available as supplementary material in IJSEM Online.
The acetylene reduction assay (ARA) was used to test the isolates grown on semi-solid LGI medium (Cavalcante & Dobereiner, 1988) for potential nitrogen fixation. The amount of ethylene produced was measured using 10 % (v/v) acetylene according to the method of Li & MacRae (1992) using a Hewlett Packard 4890 GC equipped with a Poropack N column. Strains PA51T and PA12 were able to reduce acetylene to ethylene. The strains were subjected to a nifD-specific PCR amplification using the primers of Ueda et al. (1995) and the expected 450 bp amplification product was observed in both isolates. The ARA and nifD amplification results confirmed that the isolates were nitrogen fixers.
Isolates PA12 and PA51T were also tested for their mineral phosphate solubilization activity. Individual strains were grown in LGI medium and 10 µl grown cells were spotted onto Pikovskaya's medium (Pikovskaya, 1948) and the zonal clearing generated was measured. Isolates PA12 and PA51T showed clearing zones on the medium, indicating that these strains were capable of solubilizing the tri-calcium phosphates contained in the medium.
The polyphasic study of acetic acid bacteria isolated from Porteresia coarctata has revealed the following characteristics. Cells of all isolates were Gram-negative, rod-shaped, approximately 0·7–0·9x1·9–3·1 µm and motile with peritrichous flagella. Strains were aerobic and able to fix atmospheric nitrogen micro-aerophilically. Colonies were initially yellowish, becoming dark orange later on, smooth and raised with an entire margin on LGI medium. The isolates were capable of acid formation from glucose and overoxidation of ethanol, produced water-soluble brown pigments in GYC medium, and were oxidase-negative and catalase-positive. It is well known that Gram-negative, rod-shaped, aerobic bacteria that oxidize ethanol to acetic acid in neutral and acidic media are candidates for members of the family Acetobacteraceae (Swings et al., 1992). Additionally, the family Acetobacteraceae can be distinguished from other 
-Proteobacteria by two internal SphI sites and one NcoI restriction site in their 16S rDNA genes (Jimenez-Salgado et al., 1997). Analysis of the 16S rDNA nucleotide sequence of the majority of the acetic acid bacterial strains reported in GenBank revealed that only a few strains lack the NcoI restriction site (nt 110) (Jimenez-Salgado et al., 1997). These restriction sites are also present in isolates PA12 and PA51T, thereby distinguishing them from the other -Proteobacteria. The BLAST search of rDNA sequences also showed that the isolates had a high similarity to members of the family Acetobacteraceae. On the basis of the phenotypic and biochemical characteristics described and restriction sites in the 16S rDNA, it can be concluded that the nitrogen-fixing, salt-tolerant strains belong to the family Acetobacteraceae.
Members of the family Acetobacteraceae are recognized for their unique ability to oxidize ethanol to acetic acid in neutral and acidic media (Swings, 1992). This family consists of the genera Acetobacter, Asaia, Gluconobacter, Gluconacetobacter, Acidomonas and the recently described Kozakia (Yamada et al., 2000, Lisdiyanti et al., 2002). The isolates described in this study could be distinguished from the six genera of acetic acid bacteria at the generic level. The representative isolates showed 16S rDNA similarity to Asaia (98·6 %) followed by Kozakia (96·5 %). Clustering on the basis of the neighbour-joining algorithm showed that isolates PA12 and PA51T formed a sublineage with type genus Asaia at a similarity level of 98·6 %. However, based on biochemical characteristics, these isolates differed from the type strains of the genus Asaia in production of acetic acid from ethanol, growth in the presence of 0·35 % acetic acid at pH 3·5, acid production from ethanol and growth in the presence of 3 % NaCl. The fatty acid 19 : 0cyclo 8c comprised 11·80 % total fatty acids in isolate PA51T, compared to 0·62–0·74 % in the genus Asaia. Furthermore, the fatty acids 10 : 0, 10 : 0 3-OH, 12 : 0, 17 : 16c, 19 : 0 10-methyl, 20 : 0, 20 : 36,9,12c,15, 20 : 46,9,12,15c and summed feature 4 (16 : 17c/15 iso 2-OH) were not found in PA51T, whereas they were present in Asaia bogorensis, and 13 : 1 AT 12–13 was present in PA51T, but not in Asaia bogorensis. All these data indicate that the isolates can be distinguished from members of the genus Asaia.
The isolates could be differentiated from the genus Acetobacter on the basis of the quinone system, as the genus Acetobacter has Q-9 and the isolates and the rest of the genus have Q-10 (Yamada et al., 1997). Although the isolates oxidized acetate and lactate to carbon dioxide and water like Gluconacetobacter and Acetobacter, they differed phylogenetically from these genera and from the genus Gluconobacter, and were most closely related to the genus Asaia. The isolates also differed from the genus Acidomonas, since they did not utilize methanol as a sole source of carbon.
The isolates were able to grow well in the presence of 1 % KNO3. These data indicate that the isolates may be distinguished biochemically from the genera Asaia, Acetobacter, Gluconobacter, Gluconacetobacter and Kozakia. Interestingly, the isolates were able to grow well in the presence of 3 % NaCl in SM medium, which differentiates them from the other genera. Based on the above description, it is proposed that the isolates belong to a new genus and novel species for which the name Swaminathania salitolerans gen. nov., sp. nov. is proposed.
Description of Swaminathania gen. nov.
Swaminathania (swa.mi.na.tha'ni.a. N.L. fem. n. Swaminathania after Swaminathan, Indian biologist, the father of the Green Revolution in India).
Gram-negative, straight rods with round ends, approximately 0·7–0·9x1·9–3·1 µm, possesses peritrichous flagella, oxidase-negative and catalase-positive. Capable of oxidizing ethanol to acetic acid in neutral and acid conditions, glucose to acetic acid, and oxidized acetate and lactate to CO2 and water. Able to produce water-soluble brown pigments on GYC agar medium. Does not hydrolyse gelatin and starch. Grows well in the presence of 0·35 % acetic acid, 3 % NaCl and 1 % KNO3. Produces acid from L-arabinose, D-glucose, glycerol, ethanol, D-mannose, D-galactose and sorbitol. Contains 18 : 17c/9t/12t (30·41 %), 13 : 1 AT 12–13 (0·53 %) and 19 : 0cyclo 8c (11·84 %). Able to fix nitrogen and solubilize phosphate. DNA G+C content is 57·6–59·9 mol% and the major quinone is Q-10. The type species is Swaminathania salitolerans.
Description of Swaminathania salitolerans sp. nov.
Swaminathania salitolerans (sa.li.to'le.rans. L. n. sal salt; L. part. adj. tolerans tolerating; N.L. part. adj. salitolerans salt tolerating).
Characteristics are the same as those described for the genus. The type strain is PA51T (=LMG 21291T=MTCC 3852T), isolated from mangrove-associated wild rice in Pichavaram, Tamil Nadu, India.
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ACKNOWLEDGEMENTS |
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