Skip to main content

Advertisement

SpringerLink
Log in

Diverse rhizobia that nodulate two species of Kummerowia in China

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

A total of 63 bacterial strains were isolated from root nodules of Kummerowia striata and K. stipulacea grown in different geographic regions of China. These bacteria could be divided into fast-growing (FG) rhizobia and slow-growing (SG) rhizobia according to their growth rate. Genetic diversity and taxonomic relationships among these rhizobia were revealed by PCR-based 16 S rDNA RFLP and sequencing, 16 S-IGS RFLP, SDS-PAGE of whole cell soluble proteins, BOX-PCR and symbiotic gene (nifH/nodC) analyses. The symbiotic FG strains were mainly isolated from temperate regions and they were identified as four genomic species in Rhizobium and Sinorhizobium meliloti based on the consensus of grouping results. The SG strains were classified as five genomic species within Bradyrhizobium and they were mainly isolated fron the subtropic and tropical regions. The phylogenetic analyses of nifH and nodC genes showed relationships similar to that of 16 S rDNA but the symbiotic genes of Bradyrhizobium strains isolated from Kummerowia were distinct from those isolated from Arachis and soybean. These results offered evidence for rhizobial biogeography and demonstrated that the Kummerowia-nodulating ability might have evolved independently in different regions in association with distinctive genomic species of rhizobia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Blaiotta G, Moschetti G, Aponte M, Villani F, Coppola S, Deiana P, Catzeddu P (1998) Random amplified polymorphic DNA and amplified ribosomal DNA spacer polymorphism: powerful methods to differentiate Streptococcus thermophilus strains. J Appl Microbiol 85:25–36

    Article  PubMed  Google Scholar 

  • Beyhaut E, Tlusty B, van Berkum P, Graham PH (2006) Rhizobium giardinii is the microsymbiont of Illinois bundleflower (Desmanthus illinoensis (Michx.) Macmillan) in midwestern prairies. Can J Microbiol 52:903–907

    Article  PubMed  CAS  Google Scholar 

  • Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38:392–397

    Google Scholar 

  • Chen WM, Laevens S, Lee TM, Coenye T, de Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735

    PubMed  CAS  Google Scholar 

  • Chen WM, James EK, Prescott AR, Kierans M, Sprent JI (2003) Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Mol Plant Microbe Interact 16:1051–1061

    Article  PubMed  CAS  Google Scholar 

  • Cilia V, Lafay B, Christen R (1996) Sequence heterogeneities among 16S ribosomal RNA sequences and their effect on phylogenetic analyses at the species level. Mol Biol Evol 13:451–461

    PubMed  CAS  Google Scholar 

  • De Bruijn FJ (1992) Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol 58:2180–2187

    PubMed  Google Scholar 

  • De Lajudie P, Lauren-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998) Allorhizobium undicola gen. Nov., sp. Nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290

    PubMed  Google Scholar 

  • De Lajudie P, Willems A, Nick G, Mohamed TS, Torck U, Filali-Maltouf A, Kersters K, Dreyfus B, Lindström K, Gillis M (1999) Agrobacterium bv. 1 strains isolated from nodules of tropical legumes. Syst Appl Microbiol 22:119–132

    Google Scholar 

  • De Ley J, Cattoir H, Reynaerts A (1970) The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142

    Article  PubMed  Google Scholar 

  • Dreyfus B, Garcia JL, Gillis M (1988) Characterization of Azorhizobium caulinodans gen. Nov., sp. Nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Bacteriol 38:89–98

    CAS  Google Scholar 

  • Duzan HM, Zhou X, Souleimanov A, Smith DL (2004) Perception of Bradyrhizobium japonicum Nod factor by soybean [Glycine max (L.) Merr.] root hairs under abiotic stress conditions. J Exp Bot. 55:2641–2646

    Article  PubMed  CAS  Google Scholar 

  • Farrand SK, van Berkum PB, Oger P (2003) Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol 53:1681–1687

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Gao JL, Turner SL, Kan FL, Wang ET, Tan ZY, Qiu YH, Gu J, Terefework Z, Young JPW, Lindström K, Chen WX (2004) Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the northern regions of China. Int J Syst Evol Microbiol 54:2003–2012

    Article  PubMed  CAS  Google Scholar 

  • Han SZ, Wang ET, Chen WX (2005) Diverse bacteria isolated from root nodules of Phaseolus vulgaris and species within the genera Campylotropis and Cassia grown in China. Syst Appl Microbiol. 28:265–276

    Article  PubMed  CAS  Google Scholar 

  • Haukka K, Lindström K, Young JPW (1996) Diversity of partial 16 S rRNA sequences among and within strains of African rhizobia isolated from Acacia and Prosopis. Syst Appl Microbiol 19:352–359

    Google Scholar 

  • Haukka K, Lindström K, Young JPW (1998) Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolated from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64:419–426

    PubMed  CAS  Google Scholar 

  • Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol 47:895–898

    Google Scholar 

  • Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. Nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32:136–139

    Google Scholar 

  • Jordan DC (1984) Family III. Rhizobiaceae Conn 1938, 321AL. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, pp 234–256

    Google Scholar 

  • Jourand P, Giraud E, Béna G, Sy A, Willems A, Gillis M, de Lajudie P, Dreyfus B (2004) Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int J Syst Evol Microbiol 54:2269–2273

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Laguerre G, Allard MR, Revoy F, Amarger N (1994) Rapid identification of rhizobia by restriction fragment length polymorphism analysis of PCR-amplified 16 S rRNA genes. Appl Environ Microbiol 60:56–63

    PubMed  CAS  Google Scholar 

  • Laguerre G, Nour SM, Macheret V, Sanjuan JJ, 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

    PubMed  CAS  Google Scholar 

  • Marmur J (1961) A procedure for the isolation of DNA from microorganisms. J Mol Biol 3:208–218

    Article  CAS  Google Scholar 

  • Mhamdi R, Mrabet M, Laguerre G, Tiwari R, Aouani ME (2005) Colonization of Phaseolus vulgaris nodules by Agrobacterium-like strains. Can J Microbiol 51:105–111

    Article  PubMed  CAS  Google Scholar 

  • Mnasri B, Mrabet M, Laguerre G, Aouani ME, Mhamdi R (2007) Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N(2)-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch Microbiol 187:79–85

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2000) Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948–950

    Article  Google Scholar 

  • Nick G, de Lajudie P, Eardly BD, Suomalainen S, Paulin L, Zhang XP, Thompson JD, Higgins DG, Gibson TJ (1994) Clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  Google Scholar 

  • Nick G, Rasanen LA, de Lajudie P, Gillis M, Lindström K (1999) Genomic screening of rhizobia isolated from root nodules of tropical leguminous trees using DNA–DNA dot-blot hybridization and rep-PCR. Syst Appl Microbiol 22:287–299

    Google Scholar 

  • Noel KD, Brill WJ (1980) Diversity and dynamics of indigenous Rhizobium japonicum populations. Appl Environ Microbiol 40:931–938

    PubMed  Google Scholar 

  • Ormeno-Orrillo E, Vinuesa P, Zuniga-Dávila D, Martínez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from Lima bean (Phaseolus lunatus L.) in Peru. Syst Appl Microbiol 29:253–262

    Article  PubMed  CAS  Google Scholar 

  • Parker MA (2003) Genetic markers for analysing symbiotic relationships and lateral gene transfer in Neotropical bradyrhizobia. Mol Ecol 12:2447–2455

    Article  PubMed  CAS  Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Rasolomampianina R, Bailly X, Fetiarison R, Dreyfus B, de lajudie P, Avarre JC (2005) Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to alpha- and beta-Proteobacteria. Mol Ecol 14:4135–4146

    Article  PubMed  CAS  Google Scholar 

  • Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martínez-Molina E, Gillis M, Velázquez E (2003) Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 26:47–53

    Article  PubMed  CAS  Google Scholar 

  • Rivas R, Willems A, Palomo JL, Garca-Benavides P (2004) Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int J Syst Evol Microbiol 54:1271–1275

    Article  PubMed  CAS  Google Scholar 

  • Sammons DW, Adams LD, Nishizawa EE (1981) Ultrasensitive silver based color staining of polypeptides in polyacrylamide gels. Electrophoresis 2:135

    Article  CAS  Google Scholar 

  • Sarita S, Sharma PK, Priefer UB, Prell J (2005) Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiol Ecol 54:1–11

    Article  PubMed  CAS  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy—the principles and practices of numerical classification. W. H. Freeman, San Francisco

    Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gills M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220

    Article  PubMed  CAS  Google Scholar 

  • Tan ZY, Wang ET, Gao JL, Martínez-Romero E, Chen WX (1997) Phylogenetic and genetic relationships of Mesorhizobium tianshanese and related rhizobia. Int J Syst Bacteriol 47:874–879

    PubMed  CAS  Google Scholar 

  • Tan ZY, Wang ET, Peng GX, Zhu ME, Martínez-Romero E, Chen WX (1999) Characterization of bacteria isolated from wild legumes in the north-western regions of China. Int J Syst Bacteriol 49:1457–1469

    Article  PubMed  CAS  Google Scholar 

  • Terefework, Kaijalainen S, Lindström K (2001) AFLP fingerprint as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega offcinalis. J Biotechnol 91:169–180

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougim F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tool. Nucleic Acid Res 24:4867–4882

    Google Scholar 

  • Tian CF, Wang ET, Han TX, Sui XH, Chen WX (2007) Genetic diversity of rhizobia associated with Vicia faba in three ecological regions of China. Arch Microbiol. May 4 (Epub ahead of print)

  • Valverde A, Velazquez E, Fernandez-Santos F, Vizcaino N, Rivas R, Mateos PF, Martinez-Molina E, Igual JM, Willems A (2005) Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989

    Article  PubMed  CAS  Google Scholar 

  • Vandamme P, Goris J, Chen WM, De Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512

    Article  PubMed  Google Scholar 

  • Vauterin L, Vauterin P (1992) Computer-aided objective comparison of electrophoresis patterns for grouping and identification of microorganisms. Eur Microbiol 1:25–40

    Google Scholar 

  • Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  • Vinuesa P, Silva C, Werner D, Martínez-Romero E (2005a) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 34:29–54

    Article  PubMed  CAS  Google Scholar 

  • Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martínez-Romero E (2005b) Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol 28:702–716

    Article  PubMed  CAS  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Blackwell, Oxford

    Google Scholar 

  • Wang Y, Zhang Z, Ramanan N (1997) The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16 S rRNA genes. J Bacteriol 179:3270–3276

    PubMed  CAS  Google Scholar 

  • Wang HK, Xia Y, Yang ZY, Natschke SL, lee KH (1998) Recent advances in the discovery and development of flavonoids and their analogues as antitumor and anti-HIV agents. Adv Exp Med Biol 439:191–225

    PubMed  CAS  Google Scholar 

  • Wang LL, Liu J, Wang ET,Chen WX (2006) Endophytic occupation of root nodules and roots of Melilotus dentatus by Agrobacterium tumefaciens. Microb Ecol 52:436–443

    Article  PubMed  Google Scholar 

  • Wei GH, Wang ET, Tan ZY, Zhu ME, Chen WX (2002) Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52:2231–2239

    Article  PubMed  CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  • Willems A, Coopman R, Gillis M (2001a) Phylogenetic and DNA–DNA hybridization analyses of Bradyrhizobium species. Int J Syst Evol Microbiol 51:111–117

    PubMed  CAS  Google Scholar 

  • Willems A, Coopman R, Gillis M (2001b) Comparison of sequence analysis of 16S–23S rDNA spacer regions, AFLP analysis and DNA–DNA hybridizations in Bradyrhizobium. Int J Syst Evol Microbiol 51:623–632

    PubMed  CAS  Google Scholar 

  • Yang SS, Bellogin RA, Buendia A, Camacho M, Chen M, Cubo T, Daza A, Diaz CL, Espuny MR, Gutierrez R, Harteveld M, Li XH, Lyra MC, Madinabeitia N, Medina C, Miao L, Ollero FJ, Olsthoorn MM, Rodriguez DN, Santamaria C, Schlaman HR, Spaink HP, Temprano F, Thomas-Oates JE, Van Brussel AA, Vinardell JM, Xie F, Yang J, Zhang HY, Zhen J, Zhou J, Ruiz-Sainz JE (2001) Effect of pH and soybean cultivars on the quantitative analyses of soybean rhizobia populations. J Biotechnol 91:243–255

    Article  PubMed  CAS  Google Scholar 

  • Yoo HH, Kim T, Ahn S, Park JH (2005) Evaluation of the Estrogenic activity of Leguminosae plants. Biol Pharm Bull 28:538–540

    Article  PubMed  CAS  Google Scholar 

  • Young JM, Kuykendall LD, Martínez-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 51:89–103

    PubMed  CAS  Google Scholar 

  • Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H (2003) Classification and nomenclature of Agrobacterium and Rhizobium—a reply to Farrand et al. (2003). Int J Syst Evol Microbiol 53:1689–1695

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank our local collaborators in each province for their great help in the collection and isolation of the rhizobial strains. Dr. Wen Feng Chen, Dr. Xin Hua Sui and Dr. Feng Qin Wang gave us valuable suggestions and technical support. This study was financially supported by National Basic Research Program of China (973) (project no. 2006CB100206) and National Program for Basic S & T Platform Construction (project no. 2005DKA 21201-10). ETW was financially supported by the grants of SIP 20060213 and 20070538 authorized by IPN, Mexico.

Author information

Authors and Affiliations

  1. Key Laboratory of Agro-Microbial Resource and Application, Ministry of Agriculture/College of Biological Sciences, China Agricultural University, Beijing, 100094, China

    Dong Xu Lin, Chao Xin Man & Wen Xin Chen

  2. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, 11340, Mexico D.F., Mexico

    En Tao Wang

Authors
  1. Dong Xu Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao Xin Man
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. En Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wen Xin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wen Xin Chen.

Additional information

Communicated by Ursula Priefer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, D.X., Man, C.X., Wang, E.T. et al. Diverse rhizobia that nodulate two species of Kummerowia in China. Arch Microbiol 188, 495–507 (2007). https://doi.org/10.1007/s00203-007-0271-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-007-0271-4

Keywords

Search

Navigation