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Science 27 July 2001:
Vol. 293. no. 5530, pp. 668 - 672
DOI: 10.1126/science.1060966

Research Articles

The Composite Genome of the Legume Symbiont Sinorhizobium meliloti

Francis Galibert,1 Turlough M. Finan,2 Sharon R. Long,34* Alfred Pühler,5 Pia Abola,6 Frédéric Ampe,7 Frédérique Barloy-Hubler,1 Melanie J. Barnett,3 Anke Becker,5 Pierre Boistard,7 Gordana Bothe,8 Marc Boutry,9 Leah Bowser,6 Jens Buhrmester,5 Edouard Cadieu,1 Delphine Capela,17dagger Patrick Chain,2 Alison Cowie,2 Ronald W. Davis,6 Stéphane Dréano,1 Nancy A. Federspiel,6ddagger Robert F. Fisher,3 Stéphanie Gloux,1 Thérèse Godrie,10 André Goffeau,9 Brian Golding,2 Jérôme Gouzy,7 Mani Gurjal,6 Ismael Hernandez-Lucas,2 Andrea Hong,3 Lucas Huizar,6 Richard W. Hyman,6 Ted Jones,6 Daniel Kahn,7 Michael L. Kahn,11 Sue Kalman,6§ David H. Keating,34 Ernö Kiss,7 Caridad Komp,6 Valérie Lelaure,1 David Masuy,9 Curtis Palm,6 Melicent C. Peck,3 Thomas M Pohl,8 Daniel Portetelle,10 Bénédicte Purnelle,9 Uwe Ramsperger,8 Raymond Surzycki,6parallel Patricia Thébault,7 Micheline Vandenbol,10 Frank-J. Vorhölter,5 Stefan Weidner,5 Derek H. Wells,3 Kim Wong,2 Kuo-Chen Yeh,34 Jacques Batut7

The scarcity of usable nitrogen frequently limits plant growth. A tight metabolic association with rhizobial bacteria allows legumes to obtain nitrogen compounds by bacterial reduction of dinitrogen (N2) to ammonium (NH4+). We present here the annotated DNA sequence of the alpha -proteobacterium Sinorhizobium meliloti, the symbiont of alfalfa. The tripartite 6.7-megabase (Mb) genome comprises a 3.65-Mb chromosome, and 1.35-Mb pSymA and 1.68-Mb pSymB megaplasmids. Genome sequence analysis indicates that all three elements contribute, in varying degrees, to symbiosis and reveals how this genome may have emerged during evolution. The genome sequence will be useful in understanding the dynamics of interkingdom associations and of life in soil environments.

1 UMR6061-CNRS, Laboratoire de Génétique et Développement, Faculté de Médecine, 2 avenue du Pr. Léon Bernard, F-35043 Rennes cedex, France.
2 Department of Biology, McMaster University, 1280 Main Street West, Hamilton, Ontario, Canada L8S 4K1.
3 Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA.
4 Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
5 Universität Bielefeld, Biologie VI (Genetik), Universitätsstrasse 25, D-33615 Bielefeld, Germany.
6 Stanford Center for DNA Sequencing and Technology, Stanford, CA 94305, USA.
7 Laboratoire de Biologie Moléculaire des Relations Plantes-Microorganismes, UMR215-CNRS-Institut National de la Recherche Agronomique (INRA), Chemin de Borde Rouge, BP 27, F-31326 Castanet Tolosan Cedex, France.
8 GATC Biotech AG, Jakob-Stadler-Platz GmbH 7, D-78467 Konstanz, Germany.
9 Unité de Biochimie physiologique, Université Catholique de Louvain, Place Croix du Sud 2, Bte 20, B-1348 Louvain-la-Neuve, Belgium.
10 Unité de Biologie Animale et Microbienne, Faculté des Sciences Agronomiques de Gembloux, Avenue Maréchal Juin 6, B-5030 Gembloux, Belgium.
11 Institute of Biological Chemistry, Washington State University, Pullman, WA 99164, USA.
*   To whom correspondence should be addressed.

dagger    Present address: Institut Curie, 26 rue d'Ulm, 75005 Paris, France.

ddagger    Present address: Exelixis, Inc., 170 Harbor Way, Post Office Box 511, South San Francisco, CA 94083-0511, USA.

§   Present address: Incyte Genomics, 3160 Porter Drive, Palo Alto, CA 94304, USA.

parallel    Present address: Département de Biologie Moléculaire Sciences 2, Université de Genève, Geneva, Switzerland 1211.

   Present address: Institute of BioAgricultural Sciences, Academia Sinica, Nankang, Taipei, Taiwan 11529.


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Identification of Sinorhizobium meliloti Early Symbiotic Genes by Use of a Positive Functional Screen.
X.-S. Zhang and H.-P. Cheng (2006)
Appl. Envir. Microbiol. 72, 2738-2748
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BacA-Mediated Bleomycin Sensitivity in Sinorhizobium meliloti Is Independent of the Unusual Lipid A Modification..
G. P. Ferguson, A. Jansen, V. L. Marlow, and G. C. Walker (2006)
J. Bacteriol. 188, 3143-3148
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MotD of Sinorhizobium meliloti and Related {alpha}-Proteobacteria Is the Flagellar-Hook-Length Regulator and Therefore Reassigned as FliK.
E. Eggenhofer, R. Rachel, M. Haslbeck, and B. Scharf (2006)
J. Bacteriol. 188, 2144-2153
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The partitioned Rhizobium etli genome: Genetic and metabolic redundancy in seven interacting replicons.
V. Gonzalez, R. I. Santamaria, P. Bustos, I. Hernandez-Gonzalez, A. Medrano-Soto, G. Moreno-Hagelsieb, S. C. Janga, M. A. Ramirez, V. Jimenez-Jacinto, J. Collado-Vides, et al. (2006)
PNAS 103, 3834-3839
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Transformation of rhizobia with broad-host-range plasmids by using a freeze-thaw method..
E. Vincze and S. Bowra (2006)
Appl. Envir. Microbiol. 72, 2290-2293
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Regulation and Properties of PstSCAB, a High-Affinity, High-Velocity Phosphate Transport System of Sinorhizobium meliloti.
Z.-C. Yuan, R. Zaheer, and T. M. Finan (2006)
J. Bacteriol. 188, 1089-1102
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The Sinorhizobium meliloti chromosomal origin of replication.
C. D. Sibley, S. R. MacLellan, and T. Finan (2006)
Microbiology 152, 443-455
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Isolation of Poly-3-Hydroxybutyrate Metabolism Genes from Complex Microbial Communities by Phenotypic Complementation of Bacterial Mutants.
C. Wang, D. J. Meek, P. Panchal, N. Boruvka, F. S. Archibald, B. T. Driscoll, and T. C. Charles (2006)
Appl. Envir. Microbiol. 72, 384-391
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Functional characterization of the Bradyrhizobium japonicum modA and modB genes involved in molybdenum transport.
M. J. Delgado, A. Tresierra-Ayala, C. Talbi, and E. J. Bedmar (2006)
Microbiology 152, 199-207
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Characterization of a Unique Chromosomal Copper Resistance Gene Cluster from Xanthomonas campestris pv. vesicatoria.
H. Basim, G. V. Minsavage, R. E. Stall, J.-F. Wang, S. Shanker, and J. B. Jones (2005)
Appl. Envir. Microbiol. 71, 8284-8291
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sinI- and expR-Dependent Quorum Sensing in Sinorhizobium meliloti.
M. Gao, H. Chen, A. Eberhard, M. R. Gronquist, J. B. Robinson, B. G. Rolfe, and W. D. Bauer (2005)
J. Bacteriol. 187, 7931-7944
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Novel DNA Sequences from Natural Strains of the Nitrogen-Fixing Symbiotic Bacterium Sinorhizobium meliloti.
H. Guo, S. Sun, T. M. Finan, and J. Xu (2005)
Appl. Envir. Microbiol. 71, 7130-7138
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Diversification of DNA Sequences in the Symbiotic Genome of Rhizobium etli.
M. Flores, L. Morales, A. Avila, V. Gonzalez, P. Bustos, D. Garcia, Y. Mora, X. Guo, J. Collado-Vides, D. Pinero, et al. (2005)
J. Bacteriol. 187, 7185-7192
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Identification of the rctA Gene, Which Is Required for Repression of Conjugative Transfer of Rhizobial Symbiotic Megaplasmids.
D. Perez-Mendoza, E. Sepulveda, V. Pando, S. Munoz, J. Nogales, J. Olivares, M. J. Soto, J. A. Herrera-Cervera, D. Romero, S. Brom, et al. (2005)
J. Bacteriol. 187, 7341-7350
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Development of a Functional Genomics Platform for Sinorhizobium meliloti: Construction of an ORFeome.
B. K. Schroeder, B. L. House, M. W. Mortimer, S. N. Yurgel, S. C. Maloney, K. L. Ward, and M. L. Kahn (2005)
Appl. Envir. Microbiol. 71, 5858-5864
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Role of the Regulatory Gene rirA in the Transcriptional Response of Sinorhizobium meliloti to Iron Limitation.
T.-C. Chao, J. Buhrmester, N. Hansmeier, A. Puhler, and S. Weidner (2005)
Appl. Envir. Microbiol. 71, 5969-5982
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Systematic Targeted Mutagenesis of Brucella melitensis 16M Reveals a Major Role for GntR Regulators in the Control of Virulence.
V. Haine, A. Sinon, F. Van Steen, S. Rousseau, M. Dozot, P. Lestrate, C. Lambert, J.-J. Letesson, and X. De Bolle (2005)
Infect. Immun. 73, 5578-5586
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Two New Sinorhizobium meliloti LysR-Type Transcriptional Regulators Required for Nodulation.
L. Luo, S.-Y. Yao, A. Becker, S. Ruberg, G.-Q. Yu, J.-B. Zhu, and H.-P. Cheng (2005)
J. Bacteriol. 187, 4562-4572
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NodMutDB: a database for genes and mutants involved in symbiosis.
C. Mao, J. Qiu, C. Wang, T. C. Charles, and B. W. S. Sobral (2005)
Bioinformatics 21, 2927-2929
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Dispersal and Evolution of the Sinorhizobium meliloti Group II RmInt1 Intron in Bacteria that Interact with Plants.
M. Fernandez-Lopez, E. Munoz-Adelantado, M. Gillis, A. Willems, and N. Toro (2005)
Mol. Biol. Evol. 22, 1518-1528
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Nebulon: a system for the inference of functional relationships of gene products from the rearrangement of predicted operons.
S. C. Janga, J. Collado-Vides, and G. Moreno-Hagelsieb (2005)
Nucleic Acids Res. 33, 2521-2530
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Cupin-Type Phosphoglucose Isomerases (Cupin-PGIs) Constitute a Novel Metal-Dependent PGI Family Representing a Convergent Line of PGI Evolution.
T. Hansen, B. Schlichting, M. Felgendreher, and P. Schonheit (2005)
J. Bacteriol. 187, 1621-1631
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Detection of and Response to Signals Involved in Host-Microbe Interactions by Plant-Associated Bacteria.
A. Brencic and S. C. Winans (2005)
Microbiol. Mol. Biol. Rev. 69, 155-194
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Ectoine-Induced Proteins in Sinorhizobium meliloti Include an Ectoine ABC-Type Transporter Involved in Osmoprotection and Ectoine Catabolism.
M. Jebbar, L. Sohn-Bosser, E. Bremer, T. Bernard, and C. Blanco (2005)
J. Bacteriol. 187, 1293-1304
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Vibrios Commonly Possess Two Chromosomes.
K. Okada, T. Iida, K. Kita-Tsukamoto, and T. Honda (2005)
J. Bacteriol. 187, 752-757
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Glutathione Plays a Fundamental Role in Growth and Symbiotic Capacity of Sinorhizobium meliloti.
J. Harrison, A. Jamet, C. I. Muglia, G. Van de Sype, O. M. Aguilar, A. Puppo, and P. Frendo (2005)
J. Bacteriol. 187, 168-174
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