Archives of Microbiology

, Volume 201, Issue 1, pp 99–105 | Cite as

Rhizobium panacihumi sp. nov., an isolate from ginseng-cultivated soil, as a potential plant growth promoting bacterium

  • Jong-Pyo Kang
  • Yue Huo
  • Yeon-Ju KimEmail author
  • Jong-Chan Ahn
  • Joon Hurh
  • Dong-Uk Yang
  • Deok-Chun YangEmail author
Original Paper


A novel bacterial strain designated DCY116T was isolated from ginseng-cultivated soil in Gochang-gun, Republic of Korea. Strain DCY116T, belongs to the genus Rhizobium, and is closely related to Rhizobium yantingense H66T (98.3%), Neorhizobium huautlense S02T (98.2%), Rhizobium soli DS-42T (98.1%), Rhizobium smilacinae PTYR-5T (97.9%), and Neorhizobium alkalisoli CCBAU 01393T (97.9%) based on 16S rRNA gene sequence analysis. Analysis of the housekeeping genes atpD, recA, and glnII showed low levels of sequence similarity (96.8%) between strain DCY116T and other closely related species. Strain DCY116T was Gram-stain negative, motile by peritrichous flagella, rod-shaped, strictly aerobic, catalase- and oxidase-positive. Q-10 was the predominant ubiquinone. The major cellular fatty acids were identified as C16:0 and summed feature 8 (C18:1 ω7c and/or C18:1 ω6c). The major polar lipids were diphosphatidylglycerol, phosphatidylethanolamine, and an unknown lipid (L1-3). Genomic DNA G + C content of strain DCY116T was determined to be 57.2 mol%. DNA–DNA homology values between strain DCY116T and closely related species of the genus Rhizobium were lower than 40%. Strain DCY116T produced indole-3-acetic acid, siderophores, and was able to solubilize phosphate as a potential plant growth promoting bacterium. In conclusion, the results of this study support strain DCY116T as a novel species of the genus Rhizobium, for which the name Rhizobium panacihumi is proposed. The type strain is DCY116T (= KCTC 62017T = JCM 32251T).


Rhizobium panacihumi Ginseng-cultivated soil Plant growth promoting bacterium 



This study was supported by a grant from the Korea Institute of Planning & Evaluation for Technology in Food, Agriculture, Forestry & Fisheries (KIPET NO: 317007-3), Republic of Korea.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

203_2018_1578_MOESM1_ESM.pdf (501 kb)
Fig. S1. Maximum-likelihood phylogenetic tree based on 16S rRNA gene sequences (1417 bp), showing the taxonomic position of strain DCY116T in the genus Rhizobium. Bootstrap values > 50% based on 1000 replications are shown at branching points. Novosphingobium panipatense SM16T (EF424402) was used as an outgroup. Bar, 0.01 substitutions per nucleotide position. Fig. S2. Neighbor-joining phylogenetic tree based on atpD (a), recA (b) and glnII (c) genes sequences (440, 452 and 608 bp), showing the taxonomic position of strain DCY116T in the genus Rhizobium. Bootstrap values >50% based on 1000 replications are shown at branching points. Bars, 0.1 substitutions per nucleotide position. Fig. S3. Two-dimensional TLC of the total lipids of strain DCY116T (a) and Rhizobium yantingense LMG 28229T (b) stained with 5% ethanolic molybdophosphoric acid. DPG, diphosphatidylglycerol; PE, phosphatidylethanolamine; AL1-2, unidentified aminolipids; L1-7, unidentified polar lipids. Table S1. Sequence similarities (%) for 16S rRNA, atpD, recA, and glnII genes among strains of the novel and reference strains. Table S2. Negative characteristics of strain DCY116T in API ZYM, API 20NE, and API ID 32GN tests (PDF 500 KB)
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  1. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20CrossRefGoogle Scholar
  2. Bauer A, Kirby W, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496CrossRefGoogle Scholar
  3. Berge O, Lodhi A, Brandelet G, Santaella C, Roncato MA et al (2009) Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol 59:367–372CrossRefGoogle Scholar
  4. Chaintreuil C et al (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66:5437–5447CrossRefGoogle Scholar
  5. Choi KT (2008) Botanical characteristics, pharmacological effects and medicinal components of Korean Panax ginseng CA Meyer. Acta Pharmacol Sin 29:1109–1118CrossRefGoogle Scholar
  6. Díaz-Zorita M, Fernández-Canigia MV (2009) Field performance of a liquid formulation of Azospirillum brasilense on dryland wheat productivity. Eur J Soil Biol 45:3–11CrossRefGoogle Scholar
  7. 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 39:224–229Google Scholar
  8. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  9. Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–346Google Scholar
  10. Gaunt M, Turner S, Rigottier-Gois L, Lloyd-Macgilp S, Young J (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048CrossRefGoogle Scholar
  11. Hiraishi A, Ueda Y, Ishihara J, Mori T (1996) Comparative lipoquinone analysis of influent sewage and activated sludge by high-performance liquid chromatography and photodiode array detection. J Gen Appl Microbiol 42:457–469CrossRefGoogle Scholar
  12. Hunter W, Kuykendall L, Manter D (2007) Rhizobium selenireducens sp. nov.: a selenite-reducing α-Proteobacteria isolated from a bioreactor. Curr Microbiol 55:455–460CrossRefGoogle Scholar
  13. Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993CrossRefGoogle Scholar
  14. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–176Google Scholar
  15. Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A (2008) Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214CrossRefGoogle Scholar
  16. Mesbah NM, Whitman WB, Mesbah M (2011) Determination of the G + C content of prokaryotes. Methods Microbiol 38:299–324CrossRefGoogle Scholar
  17. Minnikin D, O’donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett J (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241CrossRefGoogle Scholar
  18. Nguyen NL, Kim YJ, Hoang VA, Subramaniyam S, Kang JP, Kang CH, Yang DC (2016) Bacterial diversity and community structure in Korean Ginseng Field Soil are shifted by cultivation time. PloS One 11:e0155055CrossRefGoogle Scholar
  19. Peng G, Yuan Q, Li H, Zhang W, Tan Z (2008) Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Int J Syst Evol Microbiol 58:2158–2163CrossRefGoogle Scholar
  20. Pikovskaya R (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370Google Scholar
  21. Ramana CV, Parag B, Girija K, Ram BR, Ramana VV, Sasikala C (2013) Rhizobium subbaraonis sp. nov., an endolithic bacterium isolated from beach sand. Int J Syst Evol Microbiol 63:581–585CrossRefGoogle Scholar
  22. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. MIDI Inc, NewarkGoogle Scholar
  23. Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56CrossRefGoogle Scholar
  24. Sheu SY, Huang HW, Young CC, Chen WM (2015) Rhizobium alvei sp. nov., isolated from a freshwater river. Int J Syst Evol Microbiol 65:472–478CrossRefGoogle Scholar
  25. Shokri D, Emtiazi G (2010) Indole-3-acetic acid (IAA) production in symbiotic and non-symbiotic nitrogen-fixing bacteria and its optimization by Taguchi design. Curr Microbiol 61:217–225CrossRefGoogle Scholar
  26. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  27. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefGoogle Scholar
  28. Trujillo ME, Wilems A, Abril A, Planchuelo AM, Rivas R et al (2005) Nodulation of Lupinus albus by Strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327CrossRefGoogle Scholar
  29. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefGoogle Scholar
  30. Young J, Kuykendall L, Martinez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51:89–103CrossRefGoogle Scholar
  31. Zhang X, Sun L, Ma X, Sui XH, Jiang R (2011) Rhizobium pseudoryzae sp. nov., isolated from the rhizosphere of rice. Int J Syst Evol Microbiol 61:2425–2429CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Oriental Medicinal BiotechnologyKyung Hee UniversityYonginRepublic of Korea
  2. 2.Graduate School of Biotechnology, College of Life SciencesKyung Hee UniversityYonginRepublic of Korea

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