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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asai T, Iizuka H, Komagata K (1964) The flagellation and taxonomy of genera Gluconobacter and Acetobacter with reference to the existence of intermediate strains. J Gen Appl Microbiol 10:95–126. https://doi.org/10.2323/jgam.10.95
Cleenwerck I, De Vos P, De Vuyst L (2010) Phylogeny and differentiation of species of the genus Gluconacetobacter and related taxa based on multilocus sequence analyses of housekeeping genes and reclassification of Acetobacter xylinus subsp. sucrofermentans as Gluconacetobacter sucrofermentans (Toyosaki et al. 1996) sp. nov., comb. nov. Int J Syst Evol Microbiol 60:2277–2283. https://doi.org/10.1099/ijs.0.018465-0
Dutta D, Gachhui R (2006) Novel nitrogen-fixing Acetobacter nitrogenifigens sp. nov., isolated from Kombucha tea. Int J Syst Evol Microbiol 56:1899–1903. https://doi.org/10.1099/ijs.0.64101-0
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Ezaki T, Yamamoto N, Ninomiya K, Suzuki S, Yabuuchi E (1983) Transfer of Peptococcus indolicus, Peptococcus asaccharolyticus, Peptococcus prevotii, and Peptococcus magnus to the genus Peptostreptococcus and proposal of Peptostreptococcus tetradius sp. nov. Int J Syst Evol Microbiol 33:683–698. https://doi.org/10.1099/00207713-33-4-683
Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Evol Microbiol 39:224–229. https://doi.org/10.1099/00207713-39-3-224
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Ferrer S, Manes-Lazaro R, Benavent-Gil Y, Yepez A, Pardo I (2016) Acetobacter musti sp. nov., isolated from Bobal grape must. Int J Syst Evol Microbiol 66:957–961. https://doi.org/10.1099/ijsem.0.000818
Gillis M et al (1989) Acetobacter diazotrophicus sp. nov., a nitrogen-fixing acetic acid bacterium associated with sugarcane. Int J Syst Evol Microbiol 39:361–364. https://doi.org/10.1099/00207713-39-3-361
Gosselé F, Swings J, De Ley J (1980) A rapid, simple and simultaneous detection of 2-keto-, 5-keto-and 2,5-diketogluconic acids by thin-layer chromatography in culture media of acetic acid bacteria. Zentralbl Bakteriol 1:178–181. https://doi.org/10.1016/S0172-5564(80)80039-X
Kersters K, Lisdiyanti P, Komagata K, Swings J (2006) The family Acetobacteraceae: the genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes. Springer, New York, pp 163–200. https://doi.org/10.1007/0-387-30745-1_9
Kim OS et al (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. https://doi.org/10.1099/ijs.0.038075-0
Kim M, Oh H-S, Park S-C, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
Komagata K, Suzuki K-I (1988) Lipid and cell-wall analysis in bacterial systematics. In: Colwell RR, Grigorova R (eds) Methods in microbiology, vol 19. Academic, Cambridge, pp 161–207. https://doi.org/10.1016/S0580-9517(08)70410-0
Komagata K, Iino T, Yamada Y (2014) The family Acetobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Berlin Heidelberg, pp 3–78. https://doi.org/10.1007/978-3-642-30197-1_396
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Li L et al (2014) Acetobacter sicerae sp. nov., isolated from cider and kefir, and identification of species of the genus Acetobacter by dnaK, groEL and rpoB sequence analysis. Int J Syst Evol Microbiol 64:2407–2415. https://doi.org/10.1099/ijs.0.058354-0
Li L et al (2015) Bombella intestini gen. nov., sp. nov., an acetic acid bacterium isolated from bumble bee crop. Int J Syst Evol Microbiol 65:267–273. https://doi.org/10.1099/ijs.0.068049-0
Lisdiyanti P, Kawasaki H, Seki T, Yamada Y, Uchimura T, Komagata K (2000) Systematic study of the genus Acetobacter with descriptions of Acetobacter indonesiensis sp. nov., Acetobacter tropicalis sp. nov., Acetobacter orleanensis (Henneberg 1906) comb. nov., Acetobacter lovaniensis (Frateur 1950) comb. nov., and Acetobacter estunensis (Carr 1958) comb. nov. J Gen Appl Microbiol 46:147–165. https://doi.org/10.2323/jgam.46.147
Malimas T, Thi Lan Vu H, Muramatsu Y, Yukphan P, Tanasupawat S, Yamada Y (2017) Systematics of acetic acid bacteria. In: Acetic Acid Bacteria. Food Biology Series. CRC Press, Boca Raton, pp 3–43. https://doi.org/10.1201/9781315153490-3
Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218. https://doi.org/10.1016/s0022-2836(61)80047-8
Matsuda N, Matsuda M, Notake S, Yokokawa H, Kawamura Y, Hiramatsu K, Kikuchi K (2012) Evaluation of a simple protein extraction method for species identification of clinically relevant staphylococci by matrix-assisted laser desorption ionization–time of flight mass spectrometry. J Clin Microbiol 50:3862–3866. https://doi.org/10.1128/jcm.01512-12
Muthukumarasamy R et al (2005) Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28:277–286. https://doi.org/10.1016/j.syapm.2005.01.006
Pedraza RO (2008) Recent advances in nitrogen-fixing acetic acid bacteria. Int J Food Microbiol 125:25–35. https://doi.org/10.1016/j.ijfoodmicro.2007.11.079
Pedraza RO (2016) Acetic acid bacteria as plant growth promoters. In: Matsushita K, Toyama H, Tonouchi N, Okamoto-Kainuma A (eds) Acetic acid bacteria: ecology and physiology. Springer Japan, Tokyo, pp 101–120. https://doi.org/10.1007/978-4-431-55933-7_4
Pitiwittayakul N, Yukphan P, Chaipitakchonlatarn W, Yamada Y, Theeragool G (2015) Acetobacter thailandicus sp. nov., for a strain isolated in Thailand. Ann Microbiol 65:1855–1863. https://doi.org/10.1007/s13213-014-1024-7
Pitiwittayakul N et al (2016) Acetobacter suratthanensis sp. nov., an acetic acid bacterium isolated in Thailand. Ann Microbiol 66:1157–1166. https://doi.org/10.1007/s13213-016-1200-z
Saito H, Miura KI (1963) Preparation of transforming deoxyribonucleic acid by phenol treatment. Biochim Biophys Acta 72:619–629. https://doi.org/10.1016/0926-6550(63)90386-4
Silva LR, Cleenwerck I, Rivas R, Swings J, Trujillo ME, Willems A, Velazquez E (2006) Acetobacter oeni sp. nov., isolated from spoiled red wine. Int J Syst Evol Microbiol 56:21–24. https://doi.org/10.1099/ijs.0.46000-0
Spitaels F et al (2014) Acetobacter lambici sp. nov., isolated from fermenting lambic beer. Int J Syst Evol Microbiol 64:1083–1089. https://doi.org/10.1099/ijs.0.057315-0
Swings J, Monique G, Karel K (1992) Phenotypic identification of acetic acid bacteria. Appl Environ Microbiol 29:103–110
Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128
Tamaoka J, Katayama-Fujimura Y, Kuraishi H (1983) Analysis of bacterial menaquinone mixtures by high performance liquid chromatography. J Appl Bacteriol 54:31–36. https://doi.org/10.1111/j.1365-2672.1983.tb01297.x
Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266. https://doi.org/10.1099/ijs.0.016949-0
Verlander PC (1992) Detection of horseradish peroxidase by colorimetry. In: Kricka LJ (ed) Nonisotopic DNA probe techniques. Academic Press, Boston, pp 185–201. https://doi.org/10.1016/B978-0-12-426296-6.50012-5
Vu HTL et al (2013) Nguyenibacter vanlangensis gen. nov., sp. nov., an unusual acetic acid bacterium in the α-Proteobacteria. J Gen Appl Microbiol 59:153–166. https://doi.org/10.2323/jgam.59.2_153
Vu HTL et al (2016a) Tanticharoenia aidae sp. nov., for acetic acid bacteria isolated in Vietnam. Ann Microbiol 66:417–423. https://doi.org/10.1007/s13213-015-1124-z
Vu HTL, Yukphan P, Muramatsu Y, Thao DTP, Tanaka N, Ho PT, Yamada Y (2016b) The microbial diversity of acetic acid bacteria in the south of Vietnam. Vietnam J Biotechnol 14:397–408
Yamada Y (2016) Systematics of acetic acid bacteria. In: Kazunobu Matsushita HT, Tonouchi N, Okamoto-Kainuma A (eds) Acetic acid bacteria: ecology and physiology. Springer, Tokyo, pp 1–50. https://doi.org/10.1007/978-4-431-55933-7
Yamada Y, Yukphan P (2008) Genera and species in acetic acid bacteria. Int J Food Microbiol 125:15–24. https://doi.org/10.1016/j.ijfoodmicro.2007.11.077
Yamada Y, Aida K, Ocirc UT (1969) Enzymatic studies on the oxidation of sugar and sugar alcohol. V. Ubiquinone of acetic acid bacteria and its relation to classification of Gluconobacter and Acetobacter, especially of the so-called intermediate strains. J Gen Appl Microbiol 15:181–196. https://doi.org/10.2323/jgam.15.181
Yamada Y, Okada Y, Kondo K (1976) Isolation and characterization of “polarly flagellated intermediate strains” in acetic acid bacteria. J Gen Appl Microbiol 22:237–245. https://doi.org/10.2323/jgam.22.237
Yamada Y, Hoshino K, Ishikawa T (1997) The phylogeny of acetic acid bacteria based on the partial sequences of 16S ribosomal RNA: the elevation of the subgenus Gluconoacetobacter to the generic level. Biosci Biotechnol Biochem 61:1244–1251. https://doi.org/10.1271/bbb.61.1244
Yamada Y, Hosono R, Lisdyanti P, Widyastuti Y, Saono S, Uchimura T, Komagata K (1999) Identification of acetic acid bacteria isolated from Indonesian sources, especially of isolates classified in the genus Gluconobacter. J Gen Appl Microbiol 45:23–28. https://doi.org/10.2323/jgam.45.23
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yukphan P et al (2011) Neokomagataea gen. nov., with descriptions of Neokomagataea thailandica sp. nov. and Neokomagataea tanensis sp. nov., osmotolerant acetic acid bacteria of the alpha-Proteobacteria. Biosci Biotechnol Biochem 75:419–426
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-019-01497-0