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Department of Applied Biology and Chemistry, Faculty of Applied Bioscience, Tokyo University of Agriculture, Sakuragaoka 1-1-1, Setagaya-ku, Tokyo 156-8502, Japan
Correspondence
Tai Uchimura
tai{at}nodai.ac.jp
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Present address: Research Center for Biotechnology, Indonesian Institute of Sciences, Jalan Rya Bogor km 46, Cibinong 16911, Indonesia. 
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). The species was then transferred to the genus Gluconacetobacter on the basis of ubiquinone systems and partial 16S rRNA gene sequences (Yamada et al., 1997, 1998). However, protein gel electropherograms and some phenotypic features (Gosselé et al., 1983b) had already suggested the heterogeneity of the strains comprising A. hansenii. Further, four distinct DNA–DNA homology groups were recognized in Gluconacetobacter hansenii strains (Navarro et al., 1999). Homology group I was identified as G. hansenii and the other three groups remained unnamed. Two G. hansenii strains (LMG 1517=NBRC 14822 and LMG 1689) were identified as Gluconacetobacter intermedius by partial 16S rRNA gene sequences and HaeIII and HpaII restriction profiles of the PCR-amplified 16S–23S rDNA spacer region (Tr
ek & Teuber, 2002). G. hansenii LMG 1582T was suggested to be a novel species on the basis of the above-mentioned sequences and profiles (Trek, 2002).
The aim of the present study was to reclassify ten strains previously identified as A. hansenii (=G. hansenii) (Gosselé et al., 1983b; Navarro et al., 1999) and Acetobacter pasteurianus LMG 1584 (=A. pasteurianus subsp. pasteurianus LMD 39.5) (Table 1). A. pasteurianus LMG 1584 was used throughout the present study because the strain was transferred to the genus Gluconacetobacter (Lisdiyanti et al., 2000). Gluconacetobacter entanii LTH 4560T was not used in the present study because its transportation made it very difficult to obtain (C. Hertel, Institut für Lebensmitteltechnologie, Universität Hohenheim, Stuttgart, Germany, personal communication) and it was not available from any culture collections.
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; Yamada et al., 2000). The 16S rRNA gene was amplified by PCR with two primers: 20F (5'-GATTTTGATCCTGGCTCAG-3', positions 9–27) and 1500R (5'-GTTACCTTGTTACGACTT-3', positions 1509–1429). The numbering of positions was based on the Escherichia coli numbering system (GenBank accession no. V00348; Brosius et al., 1981). The purified PCR products were sequenced directly by using an ABI PRISM BigDye Terminator Cycle Sequencing Ready Reaction kit and an ABI PRISM 310 genetic analyser. The following six primers were used: 20F, 1500R, 520F (5'-CAGCAGCCGCGGTAATAC-3', positions 519–536), 520R (5'-GTATTACCGCGGCTGCTG-3', positions 536–519), 920F (5'-AAACTAAATGAATTGACGG-3', positions 907–926) and 920R (5'-CCGTCAATTCATTTGAGTTT-3', positions 926–907). Multiple alignments were performed in the program CLUSTAL_W (Thompson et al., 1997). Distance matrices for the aligned sequences were calculated by the two-parameter method (Knuc) (Kimura, 1980). Neighbour-joining (NJ) (Saitou & Nei, 1987), maximum likelihood (ML) (Felsenstein, 1981) and maximum parsimony (MP) (Felsenstein, 1983) were employed for constructing phylogenetic trees. The robustness of individual branches of the NJ tree was estimated by bootstrapping with 1000 replicates (Felsenstein, 1985). Alignment gaps and unidentified base positions were not taken into account for the calculations. The 16S rRNA gene sequences of ten G. hansenii strains, A. pasteurianus LMG 1584, Gluconacetobacter oboediens DSM 11826T, Gluconacetobacter europaeus DSM 6160T, Gluconacetobacter xylinus JCM 7644T, G. xylinus subsp. sucrofermentans JCM 9730T (Toyosaki et al., 1995) and ‘G. xylinus subsp. nonacetoxidans’ JCM 10150 (Kojima et al., 1998) were determined in the present study. InforBIO, an e-workbench for the databasing, classification and identification of microbes, was used for the analysis of the phylogenetic trees (Sugawara et al., 2003; www.wdcm.org). Available 16S rRNA gene sequences were obtained from GenBank/EMBL/DDBJ. Species, type strains, strains and GenBank accession numbers are presented in Figs 1–3.
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). A phylogenetic tree of the strains produced by ML was a little different from those produced by NJ and MP (Fig. 3). However, all of the strains were included in the cluster of the genus Gluconacetobacter, in a broad cluster of the acetic acid bacteria (family Acetobacteraceae). Further, the species of the genus Gluconacetobacter seemed likely to be separated into two subclusters. One consisted of Gluconacetobacter swingsii, G. europaeus, Gluconacetobacter nataicola, G. xylinus, G. oboediens, G. intermedius, Gluconacetobacter rhaeticus, Gluconacetobacter saccharivorans, G. hansenii and G. entanii, and 16S rRNA gene sequence similarity was 98.1–99.9 % between the type strains of the above species. The other cluster consisted of Gluconacetobacter liquefaciens, Gluconacetobacter sacchari, Gluconacetobacter diazotrophicus, Gluconacetobacter azotocaptans and Gluconacetobacter johannae, and the 16S rRNA gene sequence similarity was 98.4–99.16 % between the type strains of these species. Further, the 16S rRNA gene sequence similarity between the two subclusters was 95.7–97.6 %.
DNA was extracted and purified as reported by Saito & Miura (1963). The medium was the same as that described previously (Navarro & Komagata, 1999). A filter-sterilized cellulase (cellulase of Trichoderma viride; Wako) solution was added to the liquid medium at a final concentration of 0.025 % for the extraction of DNA from cellulose-producing strains. The cellulase was added before cultivation. This enabled the extraction of DNA from the strains because cellulose production was prevented by cellulase. DNA–DNA hybridization was performed as described by Ezaki et al. (1989) at 50 °C, a stringent hybridization temperature. G+C contents were determined as described by Tamaoka & Komagata (1984). DNA base compositions of the strains studied fell into a range of 57–63 mol% G+C (Table 2).
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). DNA–DNA similarity group I contained G. hansenii NBRC 14820T, NBRC 14816 and NBRC 14817, and was identified as G. hansenii because these strains showed high levels of DNA–DNA similarity (80–100 %) to the type strain and one another. These strains showed 99.9–100 % 16S rRNA gene sequence similarity to one another. DNA–DNA similarity group II contained a single strain, NBRC 14815. This strain showed 99.9 % 16S rRNA gene sequence similarity to G. entanii LTH 4560T. However, NBRC 14815 should be retained as Gluconacetobacter sp. because the type strain of G. entanii was not available from any source and the DNA–DNA similarity could not be determined. This case raises a problem about the identification of such strains in the future. DNA–DNA similarity group III included LMG 1582T and LMG 1584. These strains were identical to each other and separate from other groups based on DNA–DNA similarity. Therefore, the strains were regarded as a novel species, for which the name Gluconacetobacter saccharivorans sp. nov. is proposed. LMG 1582T was previously suggested to belong to a novel species based on a partial 16S rRNA gene sequence and HaeIII and HpaII restriction profiles of the PCR-amplified 16S–23S rRNA gene spacer region (Trek, 2002). This author's suggestion was confirmed in the present study. DNA–DNA similarity group IV contained G. oboediens DSM 11826T, G. hansenii NBRC 14822, LMG 1688 and LMG 1689 and G. intermedius DSM 11804T. Their 16S rRNA gene sequence similarity was 99.9–100 % to one another. High levels of DNA–DNA similarity and the similarity of 16S rRNA gene sequence revealed a synonymous relationship between G. oboediens and G. intermedius. G. oboediens has priority over G. intermedius (Boesch et al., 1998a, b; Sokollek et al., 1998) and G. intermedius is a later heterotypic synonym of G. oboediens. As a result, this group was identified as G. oboediens. LMG 1517 (=NBRC 14822) and LMG 1689 were identified previously as G. intermedius by partial 16S rRNA gene sequences and HaeIII and HpaII restriction profiles of the PCR-amplified 16S–23S rDNA spacer region (Trek & Teuber, 2002). The present study confirmed their identification. DNA–DNA similarity group V included G. europaeus DSM 6160T, G. europaeus JK2 and NBRC 3261 and was identified as G. europaeus because these strains showed high levels of DNA–DNA similarity (70–100 %) to the type strain and one another. A high value of DNA–DNA similarity (98 %) was reported between G. europaeus DSM 6160T and strain JK2 (Trek et al., 2000). It is interesting that NBRC 3261 was maintained without notation of requirement of acetic acid in the culture collection. DNA–DNA similarity group VI contained only LMG 1536T. This strain was located together with Acetobacter sp. ITDI 2.1, which was isolated from nata de coco (Bernardo et al., 1998), and close to G. europaeus and G. xylinus strains (Figs 1, 2) with 99.7–99.9 % 16S rRNA gene sequence similarity. LMG 1536T was differentiated from G. europaeus and G. xylinus by DNA–DNA similarity. Therefore, this strain was regarded as a novel species, for which the name Gluconacetobacter nataicola sp. nov. is proposed, according to its isolation source. DNA–DNA similarity group VII included G. xylinus JCM 7644T, G. xylinus subsp. sucrofermentans JCM 9730T and ‘G. xylinus subsp. nonacetoxidans’ JCM 10150, and was identified as G. xylinus because these strains showed high levels of DNA–DNA similarity (67–100 %) to the type strain and one another. This study confirmed high levels of DNA–DNA similarity of G. xylinus strains and G. xylinus subsp. sucrofermentans as reported by Tanaka et al. (2000). Recently, G. swingsii and G. rhaeticus were described and these species were separated from the type strains of the G. xylinus branch (Dellaglio et al., 2005).
The present study emphasized that when a bacterial species was established without DNA–DNA similarity data between the strains used, such a bacterial species should be re-examined for the similarity between the strains comprising the species for the stability of nomenclature. DNA–DNA similarity is still a reliable criterion for distinguishing bacterial species when clear-cut, differential phenotypic characteristics have not yet been found among the species (Cleenwerck et al., 2002; Katsura et al., 2002; Navarro et al., 1999; Lisdiyanti et al., 2000).
Isoprenoid quinones were extracted as described by Yamada et al. (1969) and determined by HPLC (Komagata & Suzuki, 1987). Three strains (NBRC 14816, LMG 1536T and LMG 1584) and two reference strains (DSM 11804T and JK2) had ubiquinones, with Q-10 accounting for >90 % and Q-9 for <10 % of the total ubiquinones. Thus, all Gluconacetobacter strains used in the present study had Q-10 as the major quinone, in agreement with data reported previously (Navarro et al., 1999).
Phenotypic characterization of the strains studied was mostly carried out as described previously (Lisdiyanti et al., 2000). Production of acid from ethanol and oxidation of ethanol were examined by clearing around colonies (Frateur, 1950; Swings et al., 1992). Growth in the presence of 0.35 % acetic acid was examined by using AG medium. This medium was used for the separation of the species in the genera Asaia and Saccharibacter from those of the genera Acetobacter, Gluconobacter, Acidomonas, Gluconacetobacter, Kozakia and Swaminathania (Jojima et al., 2004; Katsura et al., 2001; Lisdiyanti et al., 2002; Loganathan & Nair, 2004; Yamada et al., 2000). Growth at 0, 1 and 5 % acetic acid was determined by using AE broth (Entani et al., 1985) as a basal medium because G. europaeus and G. entanii strains require acetic acid for growth and these species exhibit a strong tolerance to acetic acid (Entani et al., 1985; Schüller et al., 2000; Sievers et al., 1992). Growth on ethanol was determined by using the medium described by Gosselé et al. (1983a) (Gosselé's medium). Utilization of ammoniacal nitrogen was determined by using Hoyer–Frateur medium (De Ley & Frateur, 1974), Frateur's modified Hoyer's medium (De Ley et al., 1984) and the medium described by Asai et al. (1964) (Asai's medium). Ethanol, D-glucose or D-mannitol was used as sole carbon source for the media. Acid production from sugars and sugar alcohols was examined by using the medium described by Asai et al. (1964).
Cells of all strains studied were Gram-negative and rod-shaped, measured 0.5–1.0 by 1.0–3.0 µm and were non-motile. They were aerobic, catalase-positive and oxidase-negative. The strains did not produce a water-soluble brown pigment on the culture media used, oxidized acetate and lactate, produced acid from ethanol and grew well on mannitol agar and glutamate agar. They grew in the presence of 0.35 % acetic acid in AG medium and grew without acetic acid, but not at 1 or 5 % acetic acid, in AE broth. However, NBRC 3261 grew at 1 % acetic acid and DSM 6160T and JK2 grew even at 5 % acetic acid. Production of 5-keto-D-gluconate from D-glucose varied with the strain studied. G. hansenii strains produced acid from galactitol. G. saccharivorans produced acid from propan-1-ol. Data of other characteristics are shown in Table 3.
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), respirometry (Asai et al., 1964; Kondo & Ameyama, 1958), the dissolution of CaCO3 around colonies (Asai et al., 1964; Shimwell et al., 1960; Swings et al., 1992) or the colour change of the indicator (Carr, 1968; Swings et al., 1992). Media used for the test usually contain yeast extract, peptone or other organic substances as nitrogen sources with ethanol. However, when small amounts of acetic acid are produced in liquid media and on solid media, the acid may be masked by diffusion into the media or the buffer action of the above nitrogenous substances and may give a false-negative result. Therefore, acid production from ethanol should be evaluated cautiously and recorded correctly for the identification of acetic acid bacteria. The dissolution of CaCO3 is appropriate for the production of acid from ethanol in the light of the history of acetic acid bacteria.
The strains studied did not grow on ethanol in Gosselé's broth. In contrast, a false growth was recognized on Gosselé's agar plates because the strains studied showed scant growth on agar plates with and without ethanol. The utilization (assimilation) of or growth on organic carbon compounds means the biochemical uptake of the compounds into cellular materials, and the increase in cellular mass has been regarded as the uptake of the compounds. The increase in turbidity in liquid cultures and in colonial mass on agar media has been used as a parameter for the utilization of organic compounds. However, the media used for the utilization of carbon compounds have not been specified and some media contain yeast extract, peptone or other organic substances as nitrogen sources and growth factors, such as Gosselé's agar medium. When the medium contains much larger amounts of yeast extract or peptone than of the carbon source, these organic, nitrogenous substances may serve as the carbon source as well and often give a false-positive result. Therefore, the results obtained should be examined carefully. Media containing agar cause much more difficulty in determination of growth (Cleenwerk et al., 2002; Gosselé et al., 1983a; Swings et al., 1992). When the bacteria examined require some growth factors, defined media would be preferable to complex media for the determination of utilization of carbon compounds. Acid production from sugars and sugar alcohols is often confusing with the utilization of the organic carbon compounds. This may cause false-positive growth because basal media usually contain considerable amounts of yeast extract, such as the medium reported by Asai et al. (1964).
The strains of G. hansenii and G. saccharivorans grew well at the expense of D-glucose and D-mannitol on Hoyer–Frateur medium, Frateur's modified Hoyer's medium and Asai's medium, but did not grow at the expense of ethanol. The utilization of ammoniacal nitrogen of acetic acid bacteria has been reported to vary with carbon compound used (Gosselé et al., 1983b; Navarro et al., 1999; Shimwell, 1957). Asaia strains grew well on Hoyer–Frateur medium with D-glucose or D-mannitol as sole carbon source, but not with ethanol (Katsura et al., 2001; Lisdiyanti et al., 2000; Yamada et al., 2000; Yukphan et al., 2004). Frateuria aurantia strains are biochemically similar to acetic acid bacteria and they grow on Hoyer–Frateur medium and Frateur's modified Hoyer's medium with D-mannitol as sole carbon source, but not with ethanol or D-glucose (Lisdiyanti et al., 2003). In addition, the utilization of ammoniacal nitrogen on Hoyer–Frateur medium and Frateur's modified Hoyer's medium was recognized to be inappropriate for the identification of Acetobacter strains because some strains gave false-positive growth (Lisdiyanti et al., 2000). Therefore, the taxonomic value of the utilization of ammoniacal nitrogen is rather limited to some species or genera of acetic acid bacteria and should be examined by using several kinds of carbon compounds on defined media.
The production of cellulose varied with strains studied. Cellulose production was reported to be useful for the separation of acetic acid bacteria, particularly G. xylinus in the old descriptions of acetic acid bacteria (De Ley & Frateur, 1974; Vaughn, 1957), but some strains of G. hansenii, G. oboediens, G. xylinus and G. nataicola and Gluconacetobacter sp. NBRC 14815 also produced cellulose in the present study. Therefore, the production of cellulose is not useful for the differentiation of the species in the genus Gluconacetobacter. Pellicles produced by acetic acid bacteria do not always mean real cellulose and the production of real cellulose should be confirmed by boiling the pellicles with a dilute NaOH solution (Forng et al., 1989; Navarro et al., 1999).
Description of Gluconacetobacter saccharivorans sp. nov.
Gluconacetobacter saccharivorans (sac.cha.ri.vo'rans. L. neut. n. saccharum sugar; L. part. adj. vorans devouring; N.L. masc. adj. saccharivorans sugar-devouring).
Cells are Gram-negative and rod-shaped, measure 0.5–0.8 by 1.0–1.5 µm, occur singly or in pairs and are non-motile. Strictly aerobic, catalase-positive and oxidase-negative. Cellulose and a water-soluble brown pigment are not produced. Acetate and lactate are oxidized to CO2 and H2O. Acetic acid is produced from ethanol. Growth occurs in the presence of 0.35 % acetic acid in AG medium, but not at 1 or 5 % acetic acid in AE broth. D-glucose and D-mannitol are assimilated in Hoyer–Frateur medium, Frateur's modified Hoyer's medium and Asai's broth, but not ethanol. Dihydroxyacetone is produced from glycerol and growth occurs on mannitol agar and glutamate agar. D-gluconate and 2-keto-D-gluconate are produced from D-glucose, but 5-keto-D-gluconate and 2,5-diketogluconate are not. Acid is produced from L-arabinose, D-ribose, D-xylose, D-galactose, D-glucose, glycerol, ethanol, propan-1-ol, butan-1-ol and butan-2-ol, but not from D-fructose, L-sorbose, lactose, maltose, sucrose, raffinose, galactitol, D-mannitol, D-sorbitol or starch. The major quinone is Q-10 and the minor quinone is Q-9.
The type strain is LMG 1582T (=NRIC 0614T) and its G+C content is 61 mol%. Isolated from beet juice in Germany in 1927.
Description of Gluconacetobacter nataicola sp. nov.
Gluconacetobacter nataicola [na.ta.i'co.la. N.L. neut. n. nataum nata (a food composed of cellulose produced by acetic acid bacteria in South-East Asia); L. masc. suff. -cola inhabitant; N.L. masc. n. nataicola nata inhabitant, referring to the isolation source, nata de coco, of the type strain).
Cells are Gram-negative and rod-shaped, measure 0.5–0.8 by 1.0–1.5 µm, occur singly or in pairs and are non-motile. Strictly aerobic, catalase-positive and oxidase-negative. Cellulose is produced, but water-soluble brown pigment is not. Acetate and lactate are oxidized to CO2 and H2O. Acetic acid is produced from ethanol. Growth occurs in the presence of 0.35 % acetic acid in AG medium, but not at 1 or 5 % acetic acid in AE broth. D-Mannitol is assimilated in Hoyer–Frateur medium, Frateur's modified Hoyer's medium and Asai's broth, but not D-glucose or ethanol. Dihydroxyacetone is produced from glycerol and growth occurs on mannitol agar and glutamate agar. D-Gluconate, 2-keto-D-gluconate and 5-keto-D-gluconate are produced from D-glucose, but 2,5-diketogluconate is not. Acid is produced from L-arabinose, D-ribose, D-xylose, D-galactose, D-glucose, ethanol, butan-1-ol and butan-2-ol, but not from D-fructose, L-sorbose, lactose, maltose, sucrose, raffinose, glycerol, galactitol, D-mannitol, D-sorbitol, propan-1-ol or starch. The major quinone is Q-10 and the minor quinone is Q-9.
The type strain is LMG 1536T (=NRIC 0616T) and its G+C content is 62 mol%. Isolated from nata de coco in the Philippines.
Emended description of Gluconacetobacter hansenii (Gosselé et al. 1983) Yamada et al. 1998
Cells are Gram-negative and rod-shaped, measure 0.5–0.8 by 1.0–1.5 µm, occur singly or in pairs and are non-motile. Strictly aerobic, catalase-positive and oxidase-negative. Cellulose (with the exception of one strain) and a water-soluble brown pigment are not produced. Acetate and lactate are oxidized to CO2 and H2O. Acetic acid is produced from ethanol. Growth occurs in the presence of 0.35 % acetic acid in AG medium, but not at 1 or 5 % acetic acid in AE broth. D-mannitol and D-glucose are assimilated in Hoyer–Frateur medium, Frateur's modified Hoyer's medium and Asai's broth, but not ethanol. Dihydroxyacetone is produced from glycerol and growth occurs on mannitol agar and glutamate agar. D-Gluconate, 2-keto-D-gluconate and 5-keto-D-gluconate are produced from D-glucose, but not 2,5-diketogluconate. Acid is produced from L-arabinose, D-ribose, D-xylose, D-galactose, D-glucose, galactitol, ethanol, butan-1-ol and butan-2-ol, but not from D-fructose, L-sorbose, lactose, maltose, sucrose, glycerol, D-mannitol, D-sorbitol, propan-1-ol or starch. The major quinone is Q-10 and the minor quinone is Q-9.
The type strain is NBRC 14820T (=LMG 1527T=NCIB 8745T) and its G+C content is 62 mol%. Isolated from local vinegar in Jerusalem, Israel.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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