A phylogenetic analysis of the pSymB replicon from the Sinorhizobium meliloti genome reveals a complex evolutionary history.

Microbial genomes are thought to be mosaic, making it difficult to decipher how these genomes have evolved. Whole-genome nearest-neighbor analysis was applied to the Sinorhizobium meliloti pSymB replicon to determine its origin, the degree of horizontal transfer, and the conservation of gene order. Prediction of the nearest neighbor based on contextual information, i.e., the nearest phylogenetic neighbor of adjacent genes, provided useful information for genes for which phylogenetic relationships could not be established. A large portion of pSymB genes are most closely related to genes in the Agrobacterium tumefaciens linear chromosome, including the rep and min genes. This suggests a common origin for these replicons. Genes with the nearest neighbor from the same species tend to be grouped in "patches". Gene order within these patches is conserved, but the content of the patches is not limited to operons. These data show that 13% of pSymB genes have nearest neighbors in species that are not members of the Rhizobiaceae family (including two archaea), and that these likely represent genes that have been involved in horizontal transfer.

[1]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[2]  K. Niehaus,et al.  The two megaplasmids of Rhizobium meliloti are involved in the effective nodulation of alfalfa , 1986, Molecular and General Genetics MGG.

[3]  Estelle Jumas-Bilak,et al.  Proteobacteria Alpha Subgroup of the Unconventional Genomic Organization in The , 1998 .

[4]  L. Rothfield,et al.  A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli , 1989, Cell.

[5]  H. Ochman,et al.  Amelioration of Bacterial Genomes: Rates of Change and Exchange , 1997, Journal of Molecular Evolution.

[6]  S. Karlin,et al.  Dinucleotide relative abundance extremes: a genomic signature. , 1995, Trends in genetics : TIG.

[7]  T. Jukes,et al.  Evolutionary constraints and the neutral theory , 2005, Journal of Molecular Evolution.

[8]  S. Osawa,et al.  The guanine and cytosine content of genomic DNA and bacterial evolution. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Young,et al.  The evolution of specificity in the legume-rhizobium symbiosis. , 1989, Trends in ecology & evolution.

[10]  T. Finan,et al.  oriT-Directed Cloning of Defined Large Regions from Bacterial Genomes: Identification of theSinorhizobium meliloti pExo Megaplasmid Replicator Region , 2000, Journal of bacteriology.

[11]  K. Tamura,et al.  Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. , 1992, Molecular biology and evolution.

[12]  A. Danchin,et al.  Evidence for horizontal gene transfer in Escherichia coli speciation. , 1991, Journal of molecular biology.

[13]  S. Karlin,et al.  Over- and under-representation of short oligonucleotides in DNA sequences. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S Karlin,et al.  Heterogeneity of genomes: measures and values. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[15]  S. Salzberg,et al.  Prediction of operons in microbial genomes. , 2001, Nucleic acids research.

[16]  S. Andersson,et al.  The evolution of chronic infection strategies in the α-proteobacteria , 2004, Nature Reviews Microbiology.

[17]  J. Young,et al.  The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. , 2000, Molecular biology and evolution.

[18]  Manor Askenazi,et al.  Genome Sequence of the Plant Pathogen and Biotechnology Agent Agrobacterium tumefaciens C58 , 2001, Science.

[19]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[20]  M. Osteras,et al.  Identification of Rhizobium-specific intergenic mosaic elements within an essential two-component regulatory system of Rhizobium species , 1995, Journal of bacteriology.

[21]  H. Mori,et al.  Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. , 1999, Molecular biology and evolution.

[22]  Takashi Miyata,et al.  Molecular evolution of mRNA: A method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application , 1980, Journal of Molecular Evolution.

[23]  S Karlin,et al.  Compositional biases of bacterial genomes and evolutionary implications , 1997, Journal of bacteriology.

[24]  M. Gordon,et al.  Sequence and distribution of IS1312: evidence for horizontal DNA transfer from Rhizobium meliloti to Agrobacterium tumefaciens , 1995, Journal of bacteriology.

[25]  L. Koski,et al.  Codon bias and base composition are poor indicators of horizontally transferred genes. , 2001, Molecular biology and evolution.

[26]  Kim Wong,et al.  The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  L. Karayan,et al.  Presence of one linear and one circular chromosome in the Agrobacterium tumefaciens C58 genome , 1993, Journal of bacteriology.

[28]  J A Eisen,et al.  The Genome of the Natural Genetic Engineer Agrobacterium tumefaciens C58 , 2001, Science.

[29]  L. Koski,et al.  The Closest BLAST Hit Is Often Not the Nearest Neighbor , 2001, Journal of Molecular Evolution.

[30]  M. Osteras,et al.  Presence of a gene encoding choline sulfatase in Sinorhizobium meliloti bet operon: choline-O-sulfate is metabolized into glycine betaine. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Christopher M Thomas,et al.  Paradigms of plasmid organization , 2000, Molecular microbiology.

[32]  S. Garcia-Vallvé,et al.  Horizontal gene transfer in bacterial and archaeal complete genomes. , 2000, Genome research.

[33]  G. Pesole,et al.  Glutamine synthetase gene evolution: a good molecular clock. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Bin Wang,et al.  Limitations of Compositional Approach to Identifying Horizontally Transferred Genes , 2001, Journal of Molecular Evolution.

[35]  L. Paulin,et al.  Identification and structure of the Rhizobium galegae common nodulation genes: evidence for horizontal gene transfer. , 2001, Molecular biology and evolution.

[36]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[37]  H. Ochman,et al.  Molecular archaeology of the Escherichia coli genome. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[39]  S. Tabata,et al.  Sequence determination and characterization of the replicator region in the tumor-inducing plasmid pTiB6S3 , 1989, Journal of bacteriology.

[40]  Ronald W. Davis,et al.  The Composite Genome of the Legume Symbiont Sinorhizobium meliloti , 2001, Science.

[41]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[42]  J A Eisen,et al.  Phylogenomics: improving functional predictions for uncharacterized genes by evolutionary analysis. , 1998, Genome research.

[43]  Kim Wong,et al.  Dinucleotide compositional analysis of Sinorhizobium meliloti using the genome signature: distinguishing chromosomes and plasmids , 2002, Functional & Integrative Genomics.

[44]  J. Young,et al.  Sequence diversity of the plasmid replication gene repC in the Rhizobiaceae. , 2000, Plasmid.

[45]  H. Marchandin,et al.  Le génome des alpha-protéobactéries : complexité, réduction, diversité et fluidité , 2004 .

[46]  T. Sicheritz-Pontén,et al.  A phylogenomic approach to microbial evolution. , 2001, Nucleic acids research.

[47]  Warren C. Lathe,et al.  Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. , 2000, Genome research.