Diversity and phylogeny of rhizobia

SUMMARY Rhizobia are the bacteria that form nitrogen-fixing nodules on legumes. The current list of four rhizobium genera and 17 species is reviewed, with some comments on likely future developments in the taxonomy. Sequences of the small subunit ribosomal RNA (SSU or 16S rRNA) support the well-established subdivision of rhizobia into three genera: Rhizobium, Bradyrhizobium and Azorhizobium. These all lie within the alpha subdivision of the Proteabacteria, but on quite distinct branches, each of which also includes many bacterial species that are not rhizobia. Rhizobium, by this definition, is still broad and polyphyletic, so there have recently been suggestions that this genus should be split into four genera. SSU sequences may be the best phylogenetic tool we have, but they are not an infallible guide to evolutionary relationships, particularly among closely related species: slow evolution, recombination, intraspecinc variation and even intragenomic heterogeneity are all limitations that can be illustrated by examples from the rhizobia. It seems likely that the ability to form legume nodules was not present in the common ancestor of all rhizobia but that the nodulation genes were transferred between phylogenetically distinct bacteria, so that the phylogeny of nodulation genes will probably differ from that of the bacteria that carry them. Nitrogen fixation genes are often linked to nodulation genes, but they need not have the same evolutionary history.

[1]  L. Simon.  Phylogeny of the Glomales: deciphering the past to understand the present , 1996 .

[2]  Z. Cui,et al.  Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. , 1995, International journal of systematic bacteriology.

[3]  P. Normand,et al.  Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. , 1995, International journal of systematic bacteriology.

[4]  K. Lindström,et al.  Report from the Roundtable on Rhizobium Taxonomy , 1995 .

[5]  D. Soltis,et al.  Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  T. Whittam,et al.  Species limits in Rhizobium populations that nodulate the common bean (Phaseolus vulgaris) , 1995, Applied and environmental microbiology.

[7]  L. Paulin,et al.  Nodulation Genes of Rhizobium Galegae , 1995 .

[8]  Y. Li,et al.  Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People's Republic of China. , 1995, International journal of systematic bacteriology.

[9]  I. Tikhonovich,et al.  Nitrogen Fixation: Fundamentals and Applications , 1995, Current Plant Science and Biotechnology in Agriculture.

[10]  M. Collins,et al.  Polyphasic Taxonomy of Rhizobia: Emendation of the Genus Sinorhizobium and Description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. , 1994 .

[11]  E. Triplett,et al.  DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. , 1994, Molecular plant-microbe interactions : MPMI.

[12]  P. Normand,et al.  Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.). , 1994, International journal of systematic bacteriology.

[13]  E. Martínez-Romero.  Recent developments in Rhizobium taxonomy , 1994 .

[14]  R. Overbeek,et al.  The winds of (evolutionary) change: breathing new life into microbiology , 1994 .

[15]  J. Peter,et al.  All Those New Names: an Overview of the Molecular Phylogeny of Plant-associated Bacteria , 1994 .

[16]  P H Sneath,et al.  Evidence from Aeromonas for genetic crossing-over in ribosomal sequences. , 1993, International journal of systematic bacteriology.

[17]  M. Collins,et al.  Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. , 1993, International journal of systematic bacteriology.

[18]  L. Segovia,et al.  Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. , 1993, International journal of systematic bacteriology.

[19]  M. Yanagi,et al.  Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. , 1993, FEMS microbiology letters.

[20]  Ross A. Overbeek,et al.  The ribosomal database project , 1992, Nucleic Acids Res..

[21]  T. Devine,et al.  Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp.nov. , 1992 .

[22]  G. H. Elkan.  Taxonomy of the rhizobia , 1992 .

[23]  R. Selander,et al.  Phylogenetic position of Rhizobium sp. strain Or 191, a symbiont of both Medicago sativa and Phaseolus vulgaris, based on partial sequences of the 16S rRNA and nifH genes , 1992, Applied and environmental microbiology.

[24]  G. Fox,et al.  How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. , 1992, International journal of systematic bacteriology.

[25]  J. Young,et al.  Phylogeny of fast-growing soybean-nodulating rhizobia support synonymy of Sinorhizobium and Rhizobium and assignment to Rhizobium fredii. , 1992, International journal of systematic bacteriology.

[26]  A. Kondorosi,et al.  Transduction of plant signal molecules by the Rhizobium NodD proteins , 1991, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  J. Young,et al.  Proposed Minimal Standards for the Description of New Genera and Species of Root- and Stem-Nodulating Bacteria , 1991 .

[28]  L. Segovia,et al.  Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. , 1991, International journal of systematic bacteriology.

[29]  Ji-Liang Li,et al.  RHIZOBIUM HUAKUII SP. NOV. ISOLATED FROM THE ROOT NODULES OF ASTRAGALUS SINICUS , 1991 .

[30]  J. Young,et al.  Phylogeny of the phototrophic rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment , 1991, Journal of bacteriology.

[31]  S. Orenga,et al.  DNA Homologies among Members of the Genus Azorhizobium and Other Stem- and Root-Nodulating Bacteria Isolated from the , 1991 .

[32]  K. Lindström.  Rhizobium galegae, a new species of legume root nodule bacteria , 1989 .

[33]  Ji-Liang Li,et al.  Numerical Taxonomic Study of Fast-Growing Soybean Rhizobia and a Proposal that Rhizobium fredii Be Assigned to Sinorhizobium gen. nov. , 1988 .

[34]  G. Schilling.  Hellriegel and Wilfarth and their discovery of nitrogen fixation at Bernburg , 1988 .

[35]  A. Quispel.  Hellriegel and Wilfarth's discovery of (symbiotic) nitrogen fixation hundred years ago , 1988 .

[36]  B. Dreyfus,et al.  Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata , 1988 .

[37]  L. Materon,et al.  Some aspects of the biology of nitrogen-fixing organisms , 1987 .

[38]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[39]  M. H. Scholla,et al.  Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans , 1984 .

[40]  B. Jarvis,et al.  Rhizobium loti, a New Species of Legume Root Nodule Bacteria , 1982 .

[41]  D. C. Jordan.  NOTES: Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a Genus of Slow-Growing, Root Nodule Bacteria from Leguminous Plants , 1982 .

[42]  J. K. Wilson.  OVER FIVE HUNDRED REASONS FOR ABANDONING THE CROSS‐INOCULATION GROUPS OF THE LEGUMES , 1944 .

[43]  E. B. Fred,et al.  Root nodule bacteria and leguminous plants. , 1933 .

[44]  D. Wilson.  A laboratory manual of physiological chemistry , 1929 .

[45]  A. B. Frank,et al.  Ueber die Pilzsymbiose der Leguminosen , 1890 .