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Robinia pseudoacacia in Poland and Japan is nodulated by Mesorhizobium amorphae strains

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Abstract

Robinia pseudoacacia microsymbionts from plants growing in Poland and Japan were evaluated for phylogeny and taxonomic position by genomic approach. Based on the comparative analyses of atpD (368 bp) and dnaK (573 bp) gene sequences as well as 16S rDNA restriction analysis (RFLP-16S rDNA),R. pseudoacacia microsymbionts were identified as Mesorhizobium strains. In dnaK and atpD gene phylograms R. pseudoacacia nodulators formed robust, monophyletic clusters with Mesorhizobium species with the nucleotide sequence similarity of 91–98% and 90–98%, respectively. The classification of R. pseudoacacia rhizobia to the genus Mesorhizobium was also supported by amplified 16S rDNA restriction analysis. The studied bacteria formed common clusters with Mesorhizobium species, and their DNA patterns were identical or nearly identical to Mesorhizobium genus strains. When DNA-DNA hybridization was performed, the total DNA of the representative R. pseudoacacia rhizobia exhibited 51–75% relatedness to DNA of Mesorhizobium amorphae ICMP15022 strain and below 41% to DNA of other Mesorhizobium species. These results showed that R. pseudoacacia and M. amorphae belong to the same genomospecies. The G+C content of DNA of R. pseudoacacia two microsymbionts was 59.7 and 60.6 mol% compared to 61–64 mol% across M. amorphae strains.

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References

  • Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 18:2629–2635

    Article  CAS  Google Scholar 

  • Bailly X, Olivieri I, De Mita S, Cleyet-Marel JC, Bena G (2006) Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago. Mol Ecol 15:2719–2734

    Article  CAS  PubMed  Google Scholar 

  • Broughton WJ (2003) Roses by other names: taxonomy of the Rhizobiaceae. J Bacteriol 185:2975–2979

    Article  CAS  PubMed  Google Scholar 

  • Ch Appunu, N’Zoue A, Laguerre G (2008) Genetic diversity of native bradyrhizobiaisolated from soybeans (Glycine max L.) in different agricultural-ecological-climatic regions of India. Appl Environ Microbiol 74:5991–5996

    Article  CAS  Google Scholar 

  • Coenye T, Gevers D, Van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29:147–167

    Article  CAS  PubMed  Google Scholar 

  • de Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins MD, Lindström K, Dreyfus B, Gillis M (1998) Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol 48:369–382

    Article  PubMed  Google Scholar 

  • Eardly BD, Wang FS, van Berkum P (1996) Corresponding 16S rRNA gene segments in Rhizobiaceae and Aeromonas yield discordant phylogenies. Plant Soil 186:69–74

    Article  CAS  Google Scholar 

  • Eardly BD, Nour SM, van Berkum P, Selander RK (2005) Rhizobial 16S rRNA and dnaK genes: mosaicism and the uncertain phylogenetic placement of Rhizobium galegae. Appl Environ Microbiol 70:1328–1335

    Article  CAS  Google Scholar 

  • 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 

  • 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

    CAS  PubMed  Google Scholar 

  • Gevers D, van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29:147–167

    Article  PubMed  CAS  Google Scholar 

  • Gevers D, Dawyndt P, Vandamme P, Willems A, Vancanneyt M, Swings J, de Vos P (2006) Stepping stones towards a new prokaryotic taxonomy. Phil Trans R Soc B 361:1911–1916

    Article  PubMed  Google Scholar 

  • Goodfellow M, O’Donnell AG (1993) Roots of bacterial systematics. W: handbook of bacterial systematics. Edytorzy: M. Goodfellow i A. G. O’Donnell. Academic Press, San Diego

    Google Scholar 

  • Guo X, Flores M, Morales L, García D, Bustos B, Gonzáles V, Palacios R, Dávila G (2007) DNA diversification in two Sinorhizobium species. J Bacteriol 189:6474–6476

    Article  CAS  PubMed  Google Scholar 

  • Han TX, Han LL, Wu LJ, Chen WF, Sui XH, Ju JG, Wang ET, Chen WX (2008a) Mesorhizobium gobiense sp. nov. Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China. Int J Syst Evol Microbiol 58:2610–2618

    Article  CAS  PubMed  Google Scholar 

  • Han TX, Wang EI, Han LL, Chen WF, Sui XH, Chen WX (2008b) Molecular diversity and phylogeny of rhizobia associated with wild legumes native to Xinjiang, China. Syst Appl Microbiol 31:287–301

    Article  PubMed  CAS  Google Scholar 

  • Han TX, Wang ET, Wu LJ, Chen WF, Gu JG, ChT Gu, Chang FT, XCh Wen (2008c) Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China. Int J Syst Evol Microbiol 58:1693–1699

    Article  CAS  PubMed  Google Scholar 

  • Jarvis BD, 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, Rhizobium tianshanense, to Mesorhizobium gen. nov. Int J Syst Bacteriol 47:895–898

    Article  Google Scholar 

  • Kalita M, Małek W, Kaznowski A (2004) Analysis of genetic relationship of Sarothamnus scoparius microsymbionts and Bradyrhizobium sp. by hybridization in microdilution wells. J Biosci Bioeng 97:158–161

    CAS  PubMed  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 

  • Mierzwa B, Wdowiak-Wróbel S, Małek W (2009) Phenotypic, genomic and phylogenetic characteristics of rhizobia isolated from root nodules of Robinia pseudoacacia (black locust) growing in Poland and Japan. Arch Microbiol 191:697–710

    Article  CAS  PubMed  Google Scholar 

  • Nei MM, Li W-H (1979) Mathematical model for studying genetic variations in terms of restriction endonucleases. Proc Natl Acad Sci 76:5269–5273

    Article  CAS  PubMed  Google Scholar 

  • Nicholas KB, Nicholas HBJ (1997) GeneDoc. Pittsburgh Supercomputing Center, Pittsburgh

    Google Scholar 

  • Page RD (1996) TREE VIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156

    Article  CAS  Google Scholar 

  • Posada D, Crondall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 49:817–818

    Article  Google Scholar 

  • Rossello-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  CAS  PubMed  Google Scholar 

  • Sahgal M, Johri BN (2006) Taxonomy of rhizobia: current status. Curr Sci 90:486–487

    Google Scholar 

  • Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155–179

    Article  CAS  PubMed  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical Taxonomy. Freeman, San Francisco

    Google Scholar 

  • Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MCJ, Nesme X, Roselló-Mora R, Swings J, Trüper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047

    Article  CAS  PubMed  Google Scholar 

  • Stępkowski T, Czaplińska M, Miedzińska K, Moulin L (2003) The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst Appl Microbiol 26:483–494

    Article  PubMed  Google Scholar 

  • Stępkowski T, Hughes CE, Law IJ, Markiewicz Ł, Gurda D, Chlebicka A, Moulin L (2007) Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl Environ Microbiol 73:3254–3264

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into phe-tRNA gene. Proc Natl Acad Sci U S A 95:5145–5149

    Article  CAS  PubMed  Google Scholar 

  • Sullivan JT, Eardly BD, van Berkum P, Ronson CW (1996) Four unnamed species of nonsymbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microbiol 62:2818–2825

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ulrich A, Zaspel I (2000) Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia (L.). Microbiol 143:2997–3005

    Google Scholar 

  • van Berkum P, Beyene D, Eardly BD (1996) Phylogenetic relationships among Rhizobium species nodulating the common bean (Phaseolus vulgaris L.). Int J Syst Bacteriol 43:305–313

    Google Scholar 

  • van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD (1998) Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Bacteriol 48:13–22

    Article  PubMed  Google Scholar 

  • van Berkum P, Terefework Z, Paulin L, Suomalainen S, Lindström K (2003) Discordant phylogenies within the rrn loci of rhizobia. J Bacteriol 185:2988–2998

    Article  PubMed  CAS  Google Scholar 

  • Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martίnez-Romero E (2005a) Molecular systematic 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  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang FQ, Wang ET, Liu J, Chen Q, Sui XH, Chen WF, Chen WX (2007) Mesorhizobium albiziae sp. nov., a novel bacterium that nodulates Albizia kalkora in a subtropical region of China. Int J Syst Evol Microbiol 57:192–1199

    Article  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. Raport of ad hoc committee on reconciliation of approaches to bacterial systematic. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Wei G, Chen W, Zhu W, Ch Chen, Young JP, Bontemps C (2009) Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiol Ecol 68:320–328

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Silvester WB, Park DC, Young JM (2004) Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl Environ Microbiol 70:5980–5987

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wilson JK (1939) Leguminous plants and their associated organisms. Cornell University Agricultural Experiment Station memoir 221. Cornell University Press, Ithaca

    Google Scholar 

  • Young JM (2001) Implication of alternative classifications and horizontal gene transfer for bacterial taxonomy. Int J Syst Bacteriol 51:945–953

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the grant from Ministry of Science and Higher Education No N303 057 32/1922.

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  1. Department of Genetics and Microbiology, M. Curie-Skłodowska University, Akademicka 19 st., 20-033, Lublin, Poland

    Bożena Mierzwa, Sylwia Wdowiak-Wróbel & Wanda Małek

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  1. Bożena Mierzwa
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Correspondence to Wanda Małek.

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Mierzwa, B., Wdowiak-Wróbel, S. & Małek, W. Robinia pseudoacacia in Poland and Japan is nodulated by Mesorhizobium amorphae strains. Antonie van Leeuwenhoek 97, 351–361 (2010). https://doi.org/10.1007/s10482-010-9414-8

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