Discordant Phylogenies within the rrn Loci of Rhizobia

Abstract

It is evident from complete genome sequencing results that lateral gene transfer and recombination are essential components in the evolutionary process of bacterial genomes. Since this has important implications for bacterial systematics, the primary objective of this study was to compare estimated evolutionary relationships among a representative set of ␣-Proteobacteria by sequencing analysis of three loci within their rrn operons. Tree topologies generated with 16S rRNA gene sequences were significantly different from corresponding trees assembled with 23S rRNA gene and internally transcribed space region sequences. Besides the incongruence in tree topologies, evidence that distinct segments along the 16S rRNA gene sequences of bacteria currently classified within the genera Bradyrhizobium, Mesorhizobium and Sinorhizobium have a reticulate evolutionary history was also obtained. Our data have important implications for bacterial taxonomy, because currently most taxonomic decisions are based on comparative 16S rRNA gene sequence analysis. Since phylogenetic placement based on 16S rRNA gene sequence divergence perhaps is questionable, we suggest that the proposals of bacterial nomenclature or changes in their taxonomy that have been made may not necessarily be warranted. Accordingly, a more conservative approach should be taken in the future, in which taxonomic decisions are based on the analysis of a wider variety of loci and comparative analytical methods are used to estimate phylogenetic relationships among the genomes under consideration.Rhizobia are nitrogen-fixing bacterial symbionts of legumes that are of economic importance in low-input sustainable agriculture, agroforestry, and land reclamation. Descriptions of phenotypic and genetic variation among rhizobia have been extensive. Currently there are six genera of rhizobia, Allorhizobium, Azorhizobium, Bradyrhizobium, Rhizobium, Mesorhizobium, and Sinorhizobium, that have been proposed (65), and there is a report of a single species of Methylobacterium (of the family Methylobacteriaceae), Methylobacterium nodulans, which forms a symbiosis with specific species of Crotolaria (59). The primary criterion by which these genera are defined is analysis of 16S rRNA gene sequence (65).Sequencing the 16S rRNA gene has profoundly affected how relationships among the bacteria are portrayed (45). The 16S rRNA gene sequence is useful for this purpose because it is slowly evolving and the gene product is both universally essential and functionally conserved. However, basing bacterial phylogeny on 16S rRNA gene sequence variation not only presupposes that evolution throughout the genome progresses at a constant rate by mutation and Darwinian selection but also assumes that the evolution of the genome and of the 16S rRNA gene is strictly hierarchical. From a practical point of view this approach also requires each genome to harbor a single copy of the 16S rRNA gene or that multiple alleles within single genomes have identical sequences.Although seemingly convenient for c...

RFLP analysis of the rRNA operon of a Brazilian collection of bradyrhizobial strains from 33 legume species

“…However, in the other clusters, speciation was not clear, including strains with mixed properties of both B. japonicum and B. elkanii when the 23S rRNA was compared with the 16S rRNA and IGS regions. Therefore, the results from our study confirm that phylogenies of rhizobia based on 16S rRNA and 23S rRNA genes may be discordant (van Berkum et al, 2003).…”

Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris

“…In our strain the homologous bacteriophytochrome gene rpa1537 contains a frameshift mutation and is probably inactive. Analysis of rRNA sequences indicates that R. palustris is closely related to the A. sensitiva symbiont as well as to the soybean symbiont B. japonicum 8 . However, R. palustris has never been found in symbiotic association with plants, and its genome lacks nodulation genes.…”

Discovery of a free-living chlorophyll d -producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene

“…However, results of LGT of rrn operons be- tween enterobacteria in the laboratory (27), in which recipients suffered a substantial reduction in fitness, are consistent with the expectation that such events are typically deleterious, and it has remained controversial whether highly conserved loci including the SSU rRNA gene belong to a genomic core that is recalcitrant to LGT in nature (28)(29)(30)(31)(32)(33)(34). Still, possible examples of LGT of SSU rRNA-encoding DNA in nature have been reported based on patterns of rrn sequence heterogeneity, but these are limited to relatively closely related organisms, including halophilic Archaea (35), rhizobia (36), and certain actinomycetes (37-39). Our conclusion that an ancestor of extant Chl d-producing cyanobacteria acquired SSU rRNA-encoding DNA from a proteobacterium by LGT is therefore unprecedented for this locus in nature with respect to the astonishing evolutionary distance between donor and recipient lineages.…”