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Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography

¹ Université de Lyon, Unité Mixte de Recherche, Centre National de la Recherche Scientifique (UMR CNRS), 5557 Ecologie Microbienne, IFR41 Bio Environnement et Santé, Université Lyon I, Villeurbanne 69622 cedex, France; ² Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06279, USA; ³ Department of Microbiology, University of New Hampshire, Durham, New Hampshire, 03824, USA; ⁴ Department of Plant Sciences, University of California, Davis, California 95616, USA; ⁵ l’Institut National de la Recherche Agronomique–Unité de Recherche en Génomique Végétale (INRA-URGV), 91057 Evry cedex, France; ⁶ Genoscope, Centre National de Séquençage, 91057 Evry cedex, France; ⁷ Genoscope,CNRS-UMR 8030, Atelier de Génomique Comparative, 91006 Evry cedex, France; ⁸ Bioinformatics and Evolutionary Genomics Laboratory, UMR CNRS 5558, Université Lyon I, Villeurbanne 69622 cedex, France; ⁹ DOE Joint Genome Institute, Walnut Creek, California 94598, USA; ¹⁰ Department of Biochemistry & Cellular & Molecular Biology and The Genome Science & Technology Program, The University of Tennessee, Knoxville, Tennessee 37996, USA; ¹¹ Department of Plant Physiology, Umeå University, S-90187 Umeå, Sweden; ¹² Instituto de Biologia Molecular e Celular, Universidade do Porto, 4150-180 Porto, Portugal; ¹³ Clemson University Genomics Institute, Clemson, South Carolina 29634, USA; ¹⁴ Programa Interacciones Biológicas, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Bernal B1876BXD, Argentina

Soil bacteria that also form mutualistic symbioses in plants encounter two major levels of selection. One occurs during adaptation to and survival in soil, and the other occurs in concert with host plant speciation and adaptation. Actinobacteria from the genus Frankia are facultative symbionts that form N₂-fixing root nodules on diverse and globally distributed angiosperms in the "actinorhizal" symbioses. Three closely related clades of Frankia sp. strains are recognized; members of each clade infect a subset of plants from among eight angiosperm families. We sequenced the genomes from three strains; their sizes varied from 5.43 Mbp for a narrow host range strain (Frankia sp. strain HFPCcI3) to 7.50 Mbp for a medium host range strain (Frankia alni strain ACN14a) to 9.04 Mbp for a broad host range strain (Frankia sp. strain EAN1pec.) This size divergence is the largest yet reported for such closely related soil bacteria (97.8%–98.9% identity of 16S rRNA genes). The extent of gene deletion, duplication, and acquisition is in concert with the biogeographic history of the symbioses and host plant speciation. Host plant isolation favored genome contraction, whereas host plant diversification favored genome expansion. The results support the idea that major genome expansions as well as reductions can occur in facultative symbiotic soil bacteria as they respond to new environments in the context of their symbioses.

E-mail david.benson{at}uconn.edu; fax 860-486-4331.

[The genome sequences for Frankia strains CcI3, ACN14a, and EAN1pec have been submitted to GenBank under accession nos. CP000249, CT573213, and AAII00000000, respectively.]

Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.5798407

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