Skip to main content
Log in

Rhizobium smilacinae sp. nov., an endophytic bacterium isolated from the leaf of Smilacina japonica

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

During a study of endophytic bacteria from traditional Chinese medicinal plants, a bacterial strain, designated PTYR-5T, was isolated from the leaf of Smilacina japonica A. Gray collected from Taibai Mountain in Shaanxi Province, north-west China. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain PTYR-5T is a member of the genus Rhizobium, exhibiting the highest sequence similarities to R. cellulosilyticum LMG 23642T (97.2 %), R. huautlense LMG 18254T (97.2 %) and R. alkalisoli CCBAU 01393T (97.1 %). The levels of 16S rRNA gene sequence similarity with respect to other Rhizobium species with validly published names were less than 97.0 %. Phylogenies of the housekeeping genes atpD, recA and glnII confirmed its distinct position, showing low similarity with respect to those of recognized Rhizobium species (no more than 94.1 , 90.0 and 88.0      % similarity, respectively). The DNA–DNA relatedness values of strain PTYR-5T with R. cellulosilyticum LMG 23642T, R. huautlense LMG 18254T and R. alkalisoli CCBAU 01393T were 33.6, 21.4 and 29.5 %, respectively. Based on phenotypic, phylogenetic and genotypic data, strain PTYR-5T is considered to represent a novel species of the genus Rhizobium, for which the name Rhizobium smilacinae sp. nov. is proposed. The type strain is PTYR-5T (=CCTCC AB 2013016T=KCTC 32300T=LMG 27604T).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47:996–1006

    Article  CAS  PubMed  Google Scholar 

  • Bibi F, Chung EJ, Khan A, Jeon CO, Chung YR (2012) Rhizobium halophytocola sp. nov., isolated from the root of a coastal dune plant. Int J Syst Evol Microbiol 62:1997–2003

    Article  CAS  PubMed  Google Scholar 

  • Cleenwerck I, Vandemeulebroecke K, Janssens D, Swings J (2002) Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol 52:1551–1558

    Article  CAS  PubMed  Google Scholar 

  • Doetsch RN (1981) Determinative methods of light microscopy. In: Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GH (eds) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC, pp 21–33

    Google Scholar 

  • Euzéby JP (2014) List of prokaryotic names with standing in nomenclature. http://www.bacterio.cict.fr/

  • 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 Bacteriol 39:224–229

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Frank B (1889) Über die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–346 (in German)

    Google Scholar 

  • Fujita H, Aoki S, Kawaguchi M (2014) Evolutionary dynamics of nitrogen fixation in the legume–rhizobia symbiosis. PLoS ONE 9(4):e93670

    Article  PubMed Central  PubMed  Google Scholar 

  • Gao JL, Sun JG, Li Y, Wang ET, Chen WX (1994) Numerical taxonomy and DNA relatedness of tropical rhizobia isolated from Hainan Province, China. Int J Syst Bacteriol 44:151–158

    Article  Google Scholar 

  • García-Fraile P, Rivas R, Willems A, Peix A, Martens M, Martínez-Molina E, Mateos PF, Velázquez E (2007) Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int J Syst Evol Microbiol 57:844–848

    Article  PubMed  Google Scholar 

  • Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JPW (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048

    Article  CAS  PubMed  Google Scholar 

  • Hunter WJ, Kuykendall LD, Manter DK (2007) Rhizobium selenireducens sp. nov. a selenite-reducing α-Proteobacteria isolated from a bioreactor. Curr Microbiol 55:455–460

    Article  CAS  PubMed  Google Scholar 

  • Kim BC, Poo H, Lee KH, Kim MN, Kwon OY, Shin KS (2012) Mucilaginibacter angelicae sp. nov., isolated from the rhizosphere of Angelica polymorpha Maxim. Int J Syst Evol Microbiol 62:55–60

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kittiwongwattana C, Thawai C (2013) Rhizobium paknamense sp. nov., isolated from lesser duckweeds (Lemna aequinoctialis). Int J Syst Evol Microbiol 63:3823–3828

    Article  CAS  PubMed  Google Scholar 

  • 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 147:981–993

    CAS  PubMed  Google Scholar 

  • Lane DJ (1991) 16S-23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 125–175

    Google Scholar 

  • López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327

    Article  PubMed  Google Scholar 

  • Lu LY, Chen WF, Han LL, Wang ET, Chen WX (2009) Rhizobium alkalisoli sp. nov., isolated from Caragana intermedia growing in saline-alkaline soils in the north of China. Int J Syst Evol Microbiol 59:3006–3011

    Article  CAS  Google Scholar 

  • Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167

    Article  CAS  Google Scholar 

  • 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 58:2158–2163

    Article  CAS  PubMed  Google Scholar 

  • Quan ZX, Bae HS, Baek JH, Chen WF, Im WT, Lee ST (2005) Rhizobium daejeonense sp. nov., isolated from a cyanide treatment bioreactor. Int J Syst Evol Microbiol 55:2543–2549

    Article  CAS  PubMed  Google Scholar 

  • Rosenblueth M, Martinez-Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 181:337–344

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI technical note 101. MIDI Inc, Newark

    Google Scholar 

  • Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Höflich G, Hartmann A (1997) Root colonization of different plants by plant-growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63:2038–2046

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607–654

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludeña D, Mateos PF, Martínez-Molina E, Velázquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupine sp. nov. Appl Environ Microbiol 71:1318–1327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Turner SL, Young JPW (2000) The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 17:309–319

    Article  CAS  PubMed  Google Scholar 

  • Vincent JM (1970) The cultivation, isolation and maintenance of rhizobia. In: Vincentl JM (ed) A manual for the practical study of the root-nodule bacteria. Blackwell, Oxford, pp 1–13

    Google Scholar 

  • Wang ET, van Berkum P, Beyene D, Sui XH, Dorado O, Chen WX, Martinez-Romero E (1998) Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int J Syst Bacteriol 48:687–699

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Wang ET, Wu LJ, Sui XH, Li Y Jr, Chen WX (2011) Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int J Syst Evol Microbiol 61:2582–2588

    Article  PubMed  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE et al (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Wilson K (1987) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Greene Publishing and Wiley Interscience, New York, pp 241–245

    Google Scholar 

  • Yoon JH, Kang SJ, Yi HS, Oh TK, Ryu CM (2010) Rhizobium soli sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:1387–1393

    Article  CAS  PubMed  Google Scholar 

  • Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H et al (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, 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51:89–103

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Wang Y, Wei L, Wang Y, Shen X, Li S (2013) Taibaiella smilacinae gen. nov., sp. nov., an endophytic member of the family Chitinophagaceae isolated from the stem of Smilacina japonica, and emended description of Flavihumibacter petaseus. Int J Syst Evol Microbiol 63:3769–3776

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Wei L, Zhu L, Li C, Wang Y, Shen X (2014) Pseudoxanthomonas gei sp. nov., a novel endophytic bacterium isolated from the stem of Geum aleppicum. Antonie Van Leeuwenhoek 105:653–661

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (863 program, grant 2013AA102802), the National Natural Science Foundation of China (Grant No. 31100001 and 31170100) and the Natural Science Foundation of Shaanxi Province, China (Grant No. 2012JQ3006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yao Wang.

Additional information

Lei Zhang and Xu Shi have contributed equally to this work.

The GenBank/EMBL/DDBJ accession numbers for the partial 16S rRNA, atpD, recA and glnII gene sequences of strain PTYR-5T are KF551141, KF738707, KF738708 and KF738709, respectively.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 221 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, L., Shi, X., Si, M. et al. Rhizobium smilacinae sp. nov., an endophytic bacterium isolated from the leaf of Smilacina japonica . Antonie van Leeuwenhoek 106, 715–723 (2014). https://doi.org/10.1007/s10482-014-0241-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-014-0241-1

Keywords

Navigation