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

Author

Ying Wang, Chantal Schenowitz, Jeffrey P. Tomkins, Claudine Médigue, Luis Gabriel Wall, Claudio Valverde, Benoit Cournoyer, Nadia Demange, Philippe Normand, Alison M. Berry, Louis S. Tisa, Juliana E. Mastronunzio, David Vallenet, David R. Benson, Pascal Lapierre, Emilie Bagnarol, Tania Rawnsley, Nathalie Choisne, Zoé Rouy, Johann Peter Gogarten, Céline Lavire, Alla Lapidus, Nicole Alloisio, Vincent Daubin, Arnaud Couloux, Stéphane Cruveiller, Ying Huang, Carla A. Bassi, James Niemann, Maria Pilar Francino, Derek M. Bickhart, J Maréchal, Laurent Labarre, Beth C. Mullin, Fernando Tavares, Olga R. Kopp, Michele Martinez, Eugene Goltsman, Anita Sellstedt, Pierre Pujic, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL), Department of Molecular and Cell Biology, University of Connecticut (UCONN), Department of Microbiology, University of New Hampshire (UNH), Department of Plant Sciences [Davis, CA], University of California [Davis] (UC Davis), University of California-University of California, Unité de recherche en génomique végétale (URGV), Institut National de la Recherche Agronomique (INRA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Génomique métabolique (UMR 8030), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Bioinformatique, phylogénie et génomique évolutive (BPGE), Département PEGASE [LBBE] (PEGASE), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Department of Energy / Joint Genome Institute (DOE), Los Alamos National Laboratory (LANL), Department of Biochemistry & Cellular & Molecular Biology and the Genome Science & Technology Program, The University of Tennessee [Knoxville], Department of Biochemistry & Cellular 1 Molecular Biology and The Genome Science & Technology Program, Department of Plant Physiology, Umeå University, Genomics Institute, Clemson University, Departamento de Ciencia y Tecnología [Buenos Aires], Universidad Nacional de Quilmes (UNQ), Ecologie microbienne ( EM ), Centre National de la Recherche Scientifique ( CNRS ) -Ecole Nationale Vétérinaire de Lyon ( ENVL ) -Université Claude Bernard Lyon 1 ( UCBL ), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique ( INRA ) -VetAgro Sup ( VAS ), University of Connecticut ( UCONN ), University of New Hampshire ( UNH ), University of California [Davis] ( UC Davis ), Unité de recherche en génomique végétale ( URGV ), Institut National de la Recherche Agronomique ( INRA ) -Université d'Évry-Val-d'Essonne ( UEVE ) -Centre National de la Recherche Scientifique ( CNRS ), Genoscope - Centre national de séquençage [Evry] ( GENOSCOPE ), Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ), Génomique métabolique ( UMR 8030 ), Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université d'Évry-Val-d'Essonne ( UEVE ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ), Laboratoire de Biométrie et Biologie Evolutive ( LBBE ), Université Claude Bernard Lyon 1 ( UCBL ), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique ( Inria ) -Centre National de la Recherche Scientifique ( CNRS ), Department of Energy / Joint Genome Institute ( DOE ), Los Alamos National Laboratory ( LANL ), Programa Interacciones Biologicas, Departamento de Cienca y Tecnologia, Universidad Nacional de Quilmes, Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE)-Institut National de la Recherche Agronomique (INRA), Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Department of Plant Sciences [Univ California Davis] (Plant - UC Davis), and University of California (UC)-University of California (UC)

Subjects
DNA, Bacterial, Root nodule, Prophages, [SDE.BE.ECOM]Environmental Sciences/Biodiversity and Ecology/domain_sde.be.ecom, Molecular Sequence Data, Frankia, Plant Roots, Genome, Article, Actinobacteria, Evolution, Molecular, Magnoliopsida, 03 medical and health sciences, Symbiosis, Gene Duplication, Nitrogen Fixation, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Botany, Genetics, Phylogeny, Genetics (clinical), 030304 developmental biology, 2. Zero hunger, Frankia alni, [ SDE.BE ] Environmental Sciences/Biodiversity and Ecology, 0303 health sciences, Facultative, Geography, biology, 030306 microbiology, fungi, food and beverages, Sequence Analysis, DNA, 15. Life on land, biology.organism_classification, [ SDV.BBM.GTP ] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], DNA Transposable Elements, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Actinorhizal plant, [ SDE.BE.ECOM ] Environmental Sciences/Biodiversity and Ecology/domain_sde.be.ecom, Gene Deletion, Genome, Bacterial
Abstract

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.

Published
2006
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2. Differential Effects of Rare Specific Flavonoids on Compatible and Incompatible Strains in the Myrica gale-Frankia Actinorhizal Symbiosis

Author

Emilie Bagnarol, Pascale Fournier, Cédric Bertrand, Nicole Alloisio, Maria P. Fernandez, Gilles Comte, Floriant Bellvert, Jean Popovici, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Ecologie microbienne ( EM ), Centre National de la Recherche Scientifique ( CNRS ) -Ecole Nationale Vétérinaire de Lyon ( ENVL ) -Université Claude Bernard Lyon 1 ( UCBL ), and Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique ( INRA ) -VetAgro Sup ( VAS )

Subjects
Exudate, Frankia, Myrica gale, [ SDV.BBM.BM ] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, Biology, Myrica, Applied Microbiology and Biotechnology, 03 medical and health sciences, Plant Microbiology, Symbiosis, Nitrogen Fixation, Botany, medicine, Oligonucleotide Array Sequence Analysis, 030304 developmental biology, Flavonoids, Genetics, [ SDE.BE ] Environmental Sciences/Biodiversity and Ecology, 0303 health sciences, Ecology, 030306 microbiology, Gene Expression Profiling, Spectrum Analysis, fungi, food and beverages, [SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, biology.organism_classification, Genes, Bacterial, Nitrogen fixation, medicine.symptom, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Actinorhizal plant, Bacteria, Food Science, Biotechnology
Abstract

Plant secondary metabolites, and specifically phenolics, play important roles when plants interact with their environment and can act as weapons or positive signals during biotic interactions. One such interaction, the establishment of mutualistic nitrogen-fixing symbioses, typically involves phenolic-based recognition mechanisms between host plants and bacterial symbionts during the early stages of interaction. While these mechanisms are well studied in the rhizobia-legume symbiosis, little is known about the role of plant phenolics in the symbiosis between actinorhizal plants and Frankia genus strains. In this study, the responsiveness of Frankia strains to plant phenolics was correlated with their symbiotic compatibility. We used Myrica gale , a host species with narrow symbiont specificity, and a set of compatible and noncompatible Frankia strains. M. gale fruit exudate phenolics were extracted, and 8 dominant molecules were purified and identified as flavonoids by high-resolution spectroscopic techniques. Total fruit exudates, along with two purified dihydrochalcone molecules, induced modifications of bacterial growth and nitrogen fixation according to the symbiotic specificity of strains, enhancing compatible strains and inhibiting incompatible ones. Candidate genes involved in these effects were identified by a global transcriptomic approach using ACN14a strain whole-genome microarrays. Fruit exudates induced differential expression of 22 genes involved mostly in oxidative stress response and drug resistance, along with the overexpression of a whiB transcriptional regulator. This work provides evidence for the involvement of plant secondary metabolites in determining symbiotic specificity and expands our understanding of the mechanisms, leading to the establishment of actinorhizal symbioses.

Published
2010
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3. Chemical composition of essential oil and headspace-solid microextracts from fruits of Myrica gale L. and antifungal activity

Author

Emilie Bagnarol, Maria P. Fernandez, Cédric Bertrand, Gilles Comte, and Jean Popovici

Subjects
Antifungal Agents, Cladosporium cladosporioides, Myrica gale, Aspergillus flavus, Germacrone, Plant Science, Microbial Sensitivity Tests, Biochemistry, Gas Chromatography-Mass Spectrometry, Analytical Chemistry, law.invention, chemistry.chemical_compound, Species Specificity, law, Oils, Volatile, Food science, Essential oil, Limonene, Chromatography, biology, Organic Chemistry, Fungi, biology.organism_classification, Myrica, chemistry, Penicillium expansum, Gas chromatography–mass spectrometry
Abstract

The essential oil and the volatile compounds of Myrica gale fruits were analysed by gas chromatography (GC) and GC-mass spectrometry (GC-MS). The volatile compounds were detected using two different fibres for headspace-solid phase microextraction (HS-SPME), Carboxen/PDMS and PDMS. Sixty two compounds were identified, which represented more than 90% of the total extracts. Major components of fruit essential oil are alpha-pinene (22.6%), 1,8-cineole (18.9%) and germacrone (14.2%), whereas they are germacrone (25.1%), alpha-pinene (12.2%), limonene (8.1%) and alpha-phellandrene (8.0%) for the leaf essential oil. Major volatile fruit compounds detected in HS-SPME were alpha-pinene, 1,8-cineole, p-cymene and eth-cadinene. As M. gale fruits are traditionally used in brewery for flavouring beer or as a spice in soups or stews, the antifungal properties of these essential oils were investigated on a panel of foodborne fungi, namely Aspergillus flavus, Cladosporium cladosporioides and Penicillium expansum. A complete antifungal activity was observed at 1000 ppm against C. cladosporioides. Both essential oil and entire fruits could thus be used as an additive in food or cosmetic preparations for their flavour, odour and their conservative properties.

Published
2008

4. Differential Frankia protein patterns induced by phenolic extracts from Myricaceae seeds

Author

Maria P. Fernandez, J Maréchal, Petar Pujic, Jean Popovici, Emilie Bagnarol, Nicole Alloisio, Philippe Normand, Ecologie microbienne ( EM ), Centre National de la Recherche Scientifique ( CNRS ) -Ecole Nationale Vétérinaire de Lyon ( ENVL ) -Université Claude Bernard Lyon 1 ( UCBL ), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique ( INRA ) -VetAgro Sup ( VAS ), Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL), Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), and Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)

Subjects
Physiology, Frankia, Plant Science, Myricaceae, 03 medical and health sciences, chemistry.chemical_compound, Biosynthesis, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Genetics, Protein biosynthesis, 030304 developmental biology, Gel electrophoresis, 0303 health sciences, [ SDE.BE ] Environmental Sciences/Biodiversity and Ecology, biology, 030306 microbiology, Cell Biology, General Medicine, Metabolism, biology.organism_classification, chemistry, Biochemistry, [ SDV.BBM.GTP ] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Actinorhizal plant, Bacteria
Abstract

Two-dimensional gel electrophoresis was used to identify differentially displayed proteins expressed during the early symbiotic interactions between the bacterium Frankia and actinorhizal plants. Myricaceae, the most primitive actinorhizal family, was used as an experimental model to study specificity mechanisms because it includes species with either narrow or large specificity. Seed phenolic extracts from two Myricaceae species, Myrica gale, a narrow specificity host and Morella cerifera considered as a promiscuous host, were used to induce three Frankia strains ACN14a, M16467 and Ea112. The global protein pattern was altered by exposure to the plant extracts. The addition of 30 mg I -1 of seed phenolic extracts provoked the inhibition of many protein biosynthesis whereas 1 and 10 mg I -1 induced a global reprogramming of Frankia protein pattern. Changes in intensity of 11 5 spots in response to seed extracts were detected and analyzed by matrix-assisted laser desorption/ ionization time of flight mass spectrometry. Fifty proteins were efficiently identified with Frankia protein data banks deduced from the sequences of Frankia strains ACN14a and EaN1pec genomes. Differential proteins were involved in different metabolism pathways such as glycolysis and gluconeo-genesis, transcription, fatty acids, carbohydrates, coenzymes and purines metabolisms. Chaperones biosynthesis and iron transport regulation, essential for nitrogen fixation, seem to be strain dependant. Several proteins possibly involved in the regulation of nodulation were also differentially expressed. The most obvious response was the upregulation of oxidative stress proteins such as FeSOD and Tellurium resistance proteins, suggesting a reorganization of Frankia metabolism to protect against host plant defense.

Published
2007
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