- Original Article
- Published:
Acetobacter sacchari sp. nov., for a plant growth-promoting acetic acid bacterium isolated in Vietnam
Annals of Microbiology volume 69, pages 1155–1163 (2019)
Abstract
Purpose
Two bacterial strains, designated as isolates VTH-Ai14T and VTH-Ai15, that have plant growth-promoting ability were isolated during the study on acetic acid bacteria diversity in Vietnam. The phylogenetic analysis based on 16S rRNA gene sequences showed that the two isolates were located closely to Acetobacter nitrogenifigens RG1T but formed an independent cluster.
Methods
The phylogenetic analysis based on 16S rRNA gene and three housekeeping genes’ (dnaK, groEL, and rpoB) sequences were analyzed. The genomic DNA of the two isolates, VTH-Ai14T and VTH-Ai15, Acetobacter nitrogenifigens RG1T, the closest phylogenetic species, and Acetobacter aceti NBRC 14818T were hybridized and calculated the %similarity. Then, phenotypic and chemotaxonomic characteristics were determined for species’ description using the conventional method.
Results
The 16S rRNA gene and concatenated of the three housekeeping genes phylogenetic analysis suggests that the two isolates were constituted in a species separated from Acetobacter nitrogenifigens, Acetobacter aceti, and Acetobacter sicerae. The two isolates VTH-Ai14T and VTH-Ai15 showed 99.65% and 98.65% similarity of 16S rRNA gene when compared with Acetobacter nitrogenifigens and Acetobacter aceti and they were so different from Acetobacter nitrogenifigens RG1T with 56.99 ± 3.6 and 68.15 ± 1.8% in DNA-DNA hybridization, when isolates VTH-Ai14T and VTH-Ai15 were respectively labeled. Moreover, the two isolates were phenotypically distinguished from Acetobacter nitrogenifigens in growth in the presence of 0.35% acetic acid (v/v), on nitrogen-free LGI medium and D-mannitol, and in no ability to solubilize phosphate.
Conclusion
Therefore, the two isolates, VTH-Ai14T(= VTCC 910031T= BCC 67843T= TBRC 11175T= NRIC 0977T) and VTH-Ai15 (= VTCC 910032 = BCC 67844 = TBRC 11176 = NRIC 0978), can be assigned to an independent species within the genus Acetobacter, and the name of Acetobacter sacchari sp. nov. is proposed for the two isolates.
Introduction
The genus Acetobacter is the largest in the acetous group of the family Acetobacteraceae from the viewpoint of generic circumscription and includes 28 validly published species at present (Ferrer et al. 2016; Komagata et al. 2014; Li et al. 2014; Malimas et al. 2017; Pitiwittayakul et al. 2016, 2015; Spitaels et al. 2014; Yamada 2016). The genus was divided into two groups, i.e., the Acetobacter aceti group and the Acetobacter pasteurianus group phylogenetically (Yamada and Yukphan 2008). The species of the genus were characterized by the oxidation of acetate and lactate, acetic acid production from ethanol, no production of 2,5-diketo-D-gluconic acid from D-glucose, and UQ-9 as major (Komagata et al. 2014; Malimas et al. 2017).
Acetobacter diazotrophicus was first reported for acetic acid bacteria capable of nitrogen fixation (Gillis et al. 1989). However, this species was later transferred to the genus Gluconacetobacter as Gluconacetobacter diazotrophicus (Yamada et al. 1997).
The acetic acid bacteria with plant growth-promoting characteristics were additionally reported in the genus Acetobacter. Muthukumarasamy et al. (2005) isolated some nitrogen-fixing acetic acid bacteria from wetland rice cultivated in India and identified them as Acetobacter peroxydans. The type strain of Acetobacter peroxydans (LMG 1635T) was also proved to have the same characteristics as the isolates mentioned above (Muthukumarasamy et al. 2005; Pedraza 2008, 2016).
Acetobacter nitrogenifigens was the second species possessing a nitrogen-fixing ability and considered to be a plant growth-promoting bacterium as well (Dutta and Gachhui 2006; Pedraza 2008, 2016). The two nitrogen-fixing species are quite distance phylogenetically; the former was classified in the A. pasteurianus group, and the latter was in the A. aceti group.
Previously, the two Acetobacter strains, namely isolates VTH-Ai14 and VTH-Ai15, were isolated and phylogenetically located in the A. aceti group and closely related to Acetobacter nitrogenifigens (Vu et al. 2016b).
This paper describes Acetobacter sacchari sp. nov., as an additional plant growth-promoting species of the genus Acetobacter, for the two isolates that were isolated in Binh Phuoc Province, Vietnam, on January 28th, 2013.
Materials and methods
Two strains, designated as isolates VTH-Ai14 and VTH-Ai15, were isolated from the stems of sugar cane (Saccharum species) by an enrichment culture approach at pH 3.5 (Vu et al. 2013; Yamada et al. 1999). When microbial growth was seen in the medium, one loop of the culture was streaked onto an agar plate comprised of D-glucose, ethanol, peptone, yeast extract, and calcium carbonate to select acetic acid bacteria (Vu et al. 2013; Yamada et al. 1999). Acetobacter nitrogenifigens TBRC 15T (= RG1T) (Dutta and Gachhui 2006) and Acetobacter aceti NBRC 14818T were used as reference strains.
The 16S rRNA gene sequences of the two isolates were sequenced, as described previously (Vu et al. 2013). Sequenced were 1,419–1,420 bases for the two isolates. Multiple sequence alignments were made with MUSCLE (Edgar 2004). Sequence gaps and ambiguous bases were excluded. A phylogenetic tree based on 16S rRNA gene sequences of 1,275 bases was constructed by the maximum likelihood method based on DNA substitution model selected under the Bayesian Information Criterion (Kumar et al. 2016) using the program MEGA7 version 5.05 (Kumar et al. 2016). In the phylogenetic tree constructed, the type strains of Gluconobacter oxydans, Saccharibacter floricola, Neokomagataea tanensis, and Swingsia samuiensis were used as outgroups. The confidence values of individual branches were calculated by the use of bootstrap analysis of Felsenstein (Felsenstein 1985).
Calculation of sequence similarity levels was calculated using the EzBioCloud server by pairwise sequence alignment, in which all gaps were not considered (Kim et al. 2014; Kim et al. 2012; Tindall et al. 2010; Yoon et al. 2017).
Extraction and isolation of chromosomal DNAs were made by the use of the modified method of Marmur (Ezaki et al. 1983; Marmur 1961; Saito and Miura 1963). DNA base composition was determined by the method of Tamaoka and Komagata (Tamaoka and Komagata 1984). DNA-DNA hybridization was done with five wells for each reciprocal reactions (e.g., A × B and B × A) by the photobiotin-labeling method using microplate wells, as described by Ezaki and coauthors (Ezaki et al. 1989). Percent similarities in DNA-DNA hybridization were determined colorimetrically (Verlander 1992). The color density was measured at A450 on a Synergy™ HTX Multi-Mode Microplate Reader (BioTek Instruments Inc., USA). Isolated, single-stranded, and labeled DNA was hybridized with DNAs from test strains in 2 × SSC containing 50% formamide at 48 °C. The highest and the lowest values were excluded, and the mean of the remaining three values was taken as a similarity value and calculation of standard derivation.
The housekeeping genes dnaK (encoding the heat shock 70 kDa protein), groEL (encoding a 60-kDa chaperonin), and rpoB (encoding the DNA-directed RNA polymerase subunit beta) of the two isolates, VTH-Ai14T and VTH-Ai15, were partially sequenced (Cleenwerck et al. 2010; Li et al. 2014; Pitiwittayakul et al. 2015). The phylogenetic position based on the concatenated sequences of these housekeeping genes was compared with the type strains of the genus Acetobacter. The respectively concatenated sequences of 528, 579, and 573 bp of partial dnaK, groEL, and rpoB were used for constructed the phylogenetic analysis. Accession numbers of dnaK, groEL, and rpoB sequence of the type strains are according to the previous study (Cleenwerck et al. 2010; Li et al. 2014; Pitiwittayakul et al. 2015).
Whole-cell fatty acid methyl esters (FAME) of the two isolates, VTH-Ai14T and VTH-Ai15, and type strains of Acetobacter nitrogenifigens TBRC 15T were extracted and analyzed as described by Vu et al. (2016a) after grown on GECA medium for 48 h at 28 °C under aerobic conditions.
Additionally, the two isolates, VTH-Ai14T and VTH-Ai15, and Acetobacter nitrogenifigens TBRC 15T were subjected to matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) after grown in glucose-yeast extracted-peptone medium consisting of 2.0% glucose, 1.2% peptone, and 0.3% yeast extracted at 30 °C for 18 h with shaking at 200 rpm. The samples were prepared using the standard extraction method as described by Matsuda et al. (2012). Then, applied to a MicroFlex LT mass spectrometer (Bruker Daltonik), and the results were analyzed by MALDI Biotyper 4.1 software (Bruker Daltonik). Escherichia coli DH5α was used as a quality control as recommended by the manufacturer on each experiment.
Phenotypic characteristics were determined by the conventional methods (Asai et al. 1964; Gosselé et al. 1980; Kersters et al. 2006; Lisdiyanti et al. 2000; Swings et al. 1992; Yamada et al. 1999, 1976; Yukphan et al. 2011). A major isoprenoid quinone was extracted and quantitatively analyze by HPLC (Komagata and Suzuki 1988; Tamaoka et al. 1983; Yamada et al. 1969).
Results
In a phylogenetic tree deduced from the maximum likelihood method, isolates VTH-Ai14T and VTH-Ai15 formed a cluster, which was connected to the cluster of Acetobacter nitrogenifigens RG1T with the bootstrap value of 100% (Fig. 1). The resulting cluster was then connected to a cluster containing Acetobacter aceti NBRC 14818 T and Acetobacter sicerae LMG 1531T with the bootstrap value of 67%. The pairwise sequence similarities of isolate VTH-Ai14T were 100, 99.65, 98.65, 98.09, 97.87, 97.87, 97.59, 96.59, and 96.31% respectively to isolate VTH-Ai15, Acetobacter nitrogenifigens RG1T, Acetobacter aceti NBRC 14818T, Acetobacter musti Bo7T, Acetobacter estunensis NBRC 13751T, Acetobacter oeni B13T, Acetobacter sicerae LMG 1531T, Acetobacter peroxydans NBRC 13755T, and Acetobacter pasteurianus LMD 22.1T. The phylogenetic data obtained suggested that the two isolates constitute a species separate from either Acetobacter nitrogenifigens or Acetobacter aceti.
A phylogenetic relationship of isolates VTH-Ai14T and VTH-Ai15. The phylogenetic tree based on 16S rRNA gene sequences was constructed by the maximum likelihood method. The type strains of Gluconobacter oxydans, Saccharibacter floricola, Neokomagataea tanensis, and Swingsia samuiensis were used as outgroups. The numerals at the nodes of the respective branches indicate bootstrap values (%) derived from 1,000 replications. Bar, 0.02% sequence divergence
The DNA G+C contents of isolates VTH-Ai14T and VTH-Ai15 were 59.9 and 59.9 mol%, respectively (Table 1). The calculated values were so different from that of A. nitrogenifigens RG1T (64.1 mol%). The DNA-DNA similarities when the isolate VTH-Ai14T was reciprocally hybridized with VTH-Ai15 were high level at 100.00 ± 7.9% and 73.10 ± 9.3%. The DNA-DNA similarities of isolates VTH-Ai14T and VTH-Ai15 with the labeled Acetobacter nitrogenifigens TBRC 15T were 61.39 ± 8.0% and 44.21 ± 6.9%. While the isolates VTH-Ai14T and VTH-Ai15 were labeled, the DNA-DNA similarities with Acetobacter nitrogenifigens TBRC 15T were 56.99 ± 3.6% and 68.15 ± 1.8%, respectively. All the reciprocal DNA-DNA similarity between VTH-Ai14T and VTH-Ai15 with Acetobacter aceti NBRC 14818T was between 4.16 ± 0.4% and 15.80 ± 2.1%. The concatenated sequences of the three housekeeping genes (1,676 bp) were constructed with MEGA7 using the maximum likelihood model. The DNA substitution GTR+G+I was selected under the Bayesian Information Criterion (Kumar et al. 2016). The isolates VTH-Ai14T and VTH-Ai15 were grouped together and separated from Acetobacter nitrogenifigens TBRC 15T as same as the topologies of the phylogenetic tree based on the 16S rRNA gene (Fig. 2).
Maximum likelihood tree based on the concatenated sequence (1,676 bp) of dnaK (528 bp), groEL (579 bp), and rpoB (573 bp) showing the phylogenetic position of isolates VTH-Ai14T and VTH-Ai15 within the genus Acetobacter. The type strains of Gluconacetobacter liquefaciens and Granulibacter bethesdensis were used as outgroup. Numbers at branching points are percentage bootstrap values based on 1,000 replications. Bar, 0.05% sequence divergence
The major cellular fatty acid of the isolates VTH-Ai14T, VTH-Ai15, and Acetobacter nitrogenifigens TBRC 15T was C18:1ω7c at 55.94%, 57.04%, and 57.94%, respectively (Table 2).
The MALDI-TOF MS profiles of the isolate VTH-Ai14T, VTH-Ai15, and Acetobacter nitrogenifigens TBRC 15T were compared to each other and expressed by identification scores. The isolates VTH-Ai14T and VTH-Ai15 showed identification scores of 2.66 and 2.67, when comparing with VTH-Ai15 and VTH-Ai14T, respectively. While the identification score of the isolates VTH-Ai14T and VTH-Ai15 when comparing with Acetobacter nitrogenifigens TBRC 15T was only 1.88 and 1.92. The two isolates were discriminated from Acetobacter nitrogenifigens TBRC 15T according to the manufacturer’s recommended log score identification criteria (Matsuda et al. 2012). All the results obtained suggested that the isolates are genetically separated from either Acetobacter nitrogenifigens or Acetobacter aceti.
The phenotypic characteristics of isolates VTH-Ai14T and VTH-Ai15 were given in the species description of Acetobacter sacchari sp. nov. (Table 1).
Discussion
Acetobacter nitrogenifigens was first reported as a nitrogen-fixing bacterium equipped with polar flagellation and with a high G+C content of DNA (64.1 mol% G + C). In general, the G+C contents of DNA are ranged from 53.5 to 60.7 mol% in the genus Acetobacter (Komagata et al. 2014; Malimas et al. 2017). In addition, the peritrichous flagellation appears to be widely distributed in the genus (Komagata et al. 2014; Malimas et al. 2017). The present authors’ estimation of 59.7 mol% G+C and observation of peritrichous flagellation in Acetobacter nitrogenifigens TBRC 15T may be reasonable (Table 1).
The result of fatty acid composition showed that C18:1ω7c is a major fatty acid and the data were consistent with those reported for the validly published species of the genus Acetobacter reported by Ferrer et al. (2016). Although, the composition of minor fatty acid was slightly different and cannot discriminate the two isolates from the closest known species (Li et al. 2014; Spitaels et al. 2014), but the result of the two isolates is different from the other genera of acetic acid bacteria (Li et al. 2015; Vu et al. 2013; Yukphan et al. 2011).
The two isolates were phenotypically distinguished from Acetobacter nitrogenifigens in growth in the presence of 0.35% acetic acid (v/v), nitrogen-free LGI medium, and D-mannitol and in no ability to solubilize phosphate and from Acetobacter aceti in growth in the presence of 0.35% (v/v) acetic acid, nitrogen-free LGI medium, and D-mannitol and in the absence of phosphate solubility and production of 2-keto-D-gluconic acid (Komagata et al. 2014; Malimas et al. 2017). In addition, they were genetically and physiologically discriminated by DNA-DNA similarities obtained from the reciprocal DNA-DNA hybridization, MALDI-TOF MS profiles of the isolate, and the concatenated sequences of the three housekeeping genes from the type strain of Acetobacter nitrogenifigens (Ferrer et al. 2016; Li et al. 2014).
As described above, the two isolates VTH-Ai14T and VTH-Ai15 were separated phenotypically, genetically, and physiologically from either Acetobacter nitrogenifigens or Acetobacter aceti, the phylogenetically closest species (Komagata et al. 2014; Malimas et al. 2017). The two isolates can therefore be assigned to an independent species within the genus Acetobacter, and the name of Acetobacter sacchari sp. nov. is introduced for the two isolates (Table 1).
Description of Acetobacter sacchari sp. nov.
Acetobacter sacchari (sac’cha,ri. L. gen. sacchari; L. neut. n. Saccharum sugar cane, from which the two isolates were isolated).
Gram-negative short rods and motile with peritrichous flagella, measuring 0.4–0.5 × 0.6–1.5 μm. Colonies are entire, smooth, transparent, glistening, and creamy to slightly light pink. Catalase is positive, and oxidase is negative. Grows on LGI medium. Oxidize acetate and lactate. Produces acetic acid from ethanol. Does not grow in the presence of 30% D-glucose (w/v) or 1% potassium nitrate (w/v) but in the presence of 0.35% acetic acid (v/v). Does not hydrolyze starch and casein. Produces 5-keto-D-gluconate but not 2-keto-D-gluconate and 2,5-diketo-D-gluconate from D-glucose. Produces levan-like polysaccharide in the presence of 3.5% and 5% D-glucose (w/v), D-fructose, and glycerol. Produces dihydroxyacetone from glycerol. Very weak production of γ-pyrone compounds from D-glucose is shown.
Acid is produced from L-arabinose, D-xylose, D-galactose, D-glucose, D-mannose, glycerol very weakly, 1-propanol, and ethanol, but not from D-arabinose, D-fructose, L-sorbose, L-rhamnose, D-mannitol, D-sorbitol, dulcitol, myo-inositol, maltose, lactose, melibiose, sucrose, raffinose, 2-propanol, and methanol. Grows on L-arabinose weakly, D-galactose very weakly, D-glucose, D-mannose very weakly, D-fructose weakly, D-mannitol, glycerol, 1-propanol weakly (VTH-Ai15 grows), 2-propanol weakly, but not on D-arabinose, L-arabinose, D-xylose, L-rhamnose, L-sorbose, D-sorbitol, dulcitol, myo-inositol, maltose, sucrose, raffinose, and methanol.
Growth occurs at 20–37 °C, and no growth is found at 40 °C. Optimal growth temperature is at 25–33 °C. Optimal growth pH is from 3.0 to 8.0, and growth occurs at pH 2.5–8.0. Optimum growth is from 0 to 0.5% NaCl, and no growth at 2.0% NaCl.
A major isoprenoid quinone is Q-9. DNA G+C contents is 59.9 mol%. Major fatty acid composition is C18:1ω7c. The type strain is VTH-Ai14T (= VTCC 910031T = BCC 67843T = TBRC 11175T = NRIC 0977T), which was isolated from the stem of sugar cane (Saccharum species) collected in Thuận Phú, Đồng Phú, Bình Phước (GPS location is 11.59, 106.85), Vietnam, and whose DNA G+C content is 59.9 mol%.
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Vu, H.T.L., Yukphan, P., Bui, V.T.T. et al. Acetobacter sacchari sp. nov., for a plant growth-promoting acetic acid bacterium isolated in Vietnam. Ann Microbiol 69, 1155–1163 (2019). https://doi.org/10.1007/s13213-019-01497-0
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DOI: https://doi.org/10.1007/s13213-019-01497-0