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Actinorhizal symbiosis

Team leaders : NORMAND Philippe & FERNANDEZ Maria

Team :

Permanent members

ALLOISIO Nicole Research Scientist (CR), CNRS
BOUBAKRI Hasna Lecturer (MCF), UCB
FERNANDEZ Maria Professor (PR), UCB
FOURNIER Pascale Technician (T), CNRS
HAY-DE BETTIGNIES Anne-Emmanuelle Lecturer (MCF), UCB
NORMAND Philippe Research Director (DR), CNRS
PUJIC Petar Research Engineer (IR), CNRS

Non permanent members

CARRO GARCIA Lorena Post-doctoral researcher
POZZI Adrien PhD Student
SCHWOB Guillaume Doctorant

Presentations :

Bacteria of genus Frankia belong to the class of actinobacteria, sub-order Frankineae. These bacteria have a Gram positive cell wall and a large genome with a high percent of DNA bases G and C (G+C%). Other well known actinobacteria are Mycobacterium (agents of tuberculosis and leprosy) and Streptomyces (soil bacteria that synthesize numerous antibiotics). Twelve genomic groups called genomospecies have been described so far in Frankia. These bacteria have a morphology typical of actinobacteria with branched and segmented hyphae, multilocular sporangia and vesicles where nitrogenase synthesis takes place, both in vitro (photos) and in symbiosis.
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Figure 1: Frankia alni with on the left a sporangium and a vesicle, where nitrogen fixation takes place (Photo P. Normand), in the middle a scanning electron micrograph of a Frankia alni sporangium (Photos Y. Prin, LSTM Montpellier). On the right, a malachite/safranine staining highlights septa in Frankia alni (Photo P. Pujic).
These bacteria fix nitrogen in symbiosis with a large spectrum of dicotyledonous plants, collectively called actinorhizal that belong to 24 genera spread into 8 families among which the Betulaceae (alder), the Myricaceae (bayberry, bog myrtle, sweet gale), and the Casuarinaceae (she-oak, ironwood, australian pine). These plants, with their symbiotic bacteria, are collectively responsible for about 15% of the input of nitrogen biologically fixed on Earth. These actinorhizal plants are found in different ecosystems where nitrogen is limiting, for example glacial moraines, gravel slopes, volcanic ashes, mine spoils or burned forests.
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Figure 2: On the left, Alnus crispa planted in Northern Quebec to stabilize hydro dam dykes (photo M. Lessard), in the center Alnus glutinosa growing on the Rhone river banks in Lyon ; photo on the right, Hippophae rhamnoides growing above the Aiguebelette lake in Savoy (Photos P. Normand)
Actinorhizal plants are cultivated for their fruits, for instance sea buckthorn, or as ornamentals such as autumn olive. They are used to stabilize unstable slopes, to set wind breaks, interplanted with more valuable species to supply them with nitrogen. Some (Hippophae, Myrica) are used for their pharmaco-dynamic properties, as a source of vitamins, anti-oxydants, etc.
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Figure 3 : An alder root hair deformed following contact with Frankia hyphae (Photo Y. Prin, LSTM Montpellier). Photo on the right, a branched root hair of alder together with Frankia hyphae (Photo P. Pujic). This reaction is also triggered simply by the application of a Frankia cells supernatant..
Bacteria of genus Frankia have branched hyphae, multilocular sporangia and diazo-vesicles, cells specialized for nitrogen fixation due to a thick wall that forms a barrier against oxygen diffusion that would otherwise inhibit nitrogenase. Following contact with its host plant, the bacterium Frankia induces deformation of alder root hairs, penetrates roots where it induces cell divisions and eventually a perenial dichotomous nodule whence giant cortical cells are filled with Frankia cells.
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Figure 4 : A cortex swelling called « prenodule », that constitutes the first step in the establishment of the nodule, longitudinal cut of an alder nodule, stained with cotton blue in order to visualize cortical cells full of Frankia vesicles. The photo on the right shows a Dryas drummondii seedling from Gaspé (Canada) with a nodule (photos P. Normand).

Research themes :

Nos axes de recherche sont la physiologie et la génétique de l’interaction et l’évolution et l’écologie des symbioses.
Our research themes are the physiology and genetics of the interaction and evolution and ecology of symbioses. We aim to understand the physiological bases of this symbiosis by analyzing the modifications that occur upon establishment of the symbiosis. Because of the lack of genetic transformation tools for Frankia, knowledge of the genes involved in symbiosis is being carried out through study of the genome : project Genoscope. Through studies of the biodiversity and the phylogeny, at the level of the bacterial partner as well as at that of the host-plant, we aim to understand the modalities of the evolution of the symbiosis. Concerning Frankia, strains with differing hosts spectra are compared with close phylogenetic neighbors such as the acidothermophilic bacterium Acidothermus cellulolyticus recovered from hot springs in Yellowstone park and Geodermatophilus spp. recovered in different dry soils and on different surfaces.
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Figure 5: Circular representation of the Frankia alni genome, with a few known regions, in particular those involved in symbiosis : glnB/amtB involved in assimilation of ammonium, shc1 et shc2 involved in the synthesis of hopanoid lipids that form a barrier to diffusion of oxygen, hup1 and hup2 that permits recycling of hydrogen, a by-product of nitrogen fixation, sod that permits to cope with superoxide ions, suf that permits synthesis of iron-sulfur and nif that codes for nitrogenase (Normand et. coll., 2007).
We are interested in particular in the genome of Frankia alni, looking for symbiotic determinants. Given that Frankia is not genetically transformable, this aspect is broached through a gain-of-function approach in the actinobacterium Streptomyces. The first biological screen used is deformation of root hairs, the first step in the establishment of the symbiosis.
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Figure 6 : Alnus glutinosa seedlings growing in growth pouches (width 16cm) without mineral nitrogen. On the left, following inoculation with Frankia alni, there are root nodules and the seedlings have leaves and shoots that are more important. On the right, non-inoculated seedlings have small shoots but more important, longer root systems (Photo P. Pujic).
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Figure 7 : Effect of Myrica gale extracts on the growth of incompatible (A) or compatible (B et C) Frankia strains (Popovici et al., 2011).
From a larger perspective, we also aim to understand what are the effects of Frankia on ecosystems functions, and what are the modifications of the communities of soil bacteria following different treatments.

Bibliography :


  • Hay AE, et al. 2017. Control of Endophytic Frankia Sporulation by Alnus Nodule Metabolites. Molecular Plant-Microbe Interactions. 30:205-214. doi: 10.1094/MPMI-11-16-0235-R.


  • Carro L, et al. 2016. Organic acids metabolism in Frankia alni. Symbiosis. 1-12. doi: 10.1007/s13199-016-0404-0.

  • Franche C, Normand P, Pawlowski K, Tisa LS, Bogusz D. 2016. An update on research on Frankia. Symbiosis. 1-4. doi: 10.1007/s13199-016-0431-x.

  • Nouioui I, et al. 2016. Proposal of a type strain for Frankia alni (Woronin 1866) Von Tubeuf 1895, emended description of Frankia alni, and recognition of Frankia casuarinae sp. nov. and Frankia elaeagni sp. nov. International Journal of Systematic and Evolutionary Microbiology. doi: 10.1099/ijsem.0.001496.

  • Persson T, et al. 2016. The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: can D. glomerata change N-transport forms when nodulated? Symbiosis. 1-9. doi: 10.1007/s13199-016-0407-x.

  • Sarkar I, et al. 2016. Characterization of PAS domains in Frankia and selected Actinobacteria and their possible interaction with other co-domains for environmental adaptation. Symbiosis. 1-10. doi: 10.1007/s13199-016-0413-z.


  • Bertin PN, Michotey V, Normand P. 2015. Contributions of Descriptive and Functional Genomics to Microbial Ecology. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 831-846.

  • Bertrand J-C, Caumette P, Lebaron P, Normand P. 2015. The Thematic Fields of Microbial Ecology. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 3-7.

  • Boubakri H, et al. 2015. Absence of pupylation (prokaryotic ubiquitin-like protein modification) affects morphological and physiological differentiation in <i>Streptomyces coelicolor</i> . Journal of Bacteriology. JB.00591-15. doi: 10.1128/JB.00591-15.

  • Boudouresque C-F, Caumette P, Bertrand J-C, Normand P, Sime-Ngando T. 2015. Systematic and Evolution of Microorganisms: General Concepts. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 107-144.

  • Carro-Garcia L, et al. 2015. Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. The ISME Journal. doi: 10.1038/ismej.2014.257.

  • Caumette P, Bertrand J-C, Normand P. 2015. Some Historical Elements of Microbial Ecology. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 9-24.

  • Caumette P, Brochier-Armanet C, Normand P. 2015. Taxonomy and Phylogeny of Prokaryotes. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 145-190.

  • Cotin-Galvan L, et al. 2015. &lt;i&gt;In-planta&lt;/i&gt; Sporulation Capacity Enhances Infectivity and Rhizospheric Competitiveness of &lt;i&gt;Frankia&lt;/i&gt; Strains. Microbes and environments. doi: 10.1264/jsme2.ME15090.

  • Alloisio N, Kucho K, Pujic P, Normand P. 2015. The <i>Frankia alni</i> Symbiotic Transcriptome. In: Biological Nitrogen Fixation. De Bruijn, FJ. John Wiley & Sons, Inc: Hoboken, NJ, USA p. 757-768.

  • Granqvist E, et al. 2015. Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and nonlegumes. New Phytologist. n/a-n/a. doi: 10.1111/nph.13464.

  • Gtari M, et al. 2015. Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Scientific Reports. 5:13112. doi: 10.1038/srep13112.

  • Normand P, Benson DR, Tisa LS. 2015. Genome Characteristics of Frankia sp. Reflect Host Range and Host Plant Biogeography. Biological Nitrogen Fixation, 2 Volume Set. 245.

  • Normand P, Caumette P, Goulas P, Pujic P, Wisniewski-Dyé F. 2015. Adaptations of Prokaryotes to Their Biotopes and to Physicochemical Conditions in Natural or Anthropized Environments. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 293-351.

  • Normand P, Duran R, Le Roux X, Morris C, Poggiale J-C. 2015. Biodiversity and Microbial Ecosystems Functioning. In: Environmental Microbiology: Fundamentals and Applications. Bertrand, J-C, et al. Springer Netherlands p. 261-291.

  • Persson T, et al. 2015. Candidatus Frankia Datiscae Dg1, the Actinobacterial Microsymbiont of Datisca glomerata, Expresses the Canonical nod Genes nodABC in Symbiosis with Its Host Plant Börnke, F. PLOS ONE. 10:e0127630. doi: 10.1371/journal.pone.0127630.

  • Pozzi AC, et al. 2015. In-planta sporulation phenotype: a major life history trait to understand the evolution of Alnus-infective Frankia strains. Environmental Microbiology. 17:3125-3138. doi: 10.1111/1462-2920.12644.

  • Sghaier H, et al. 2015. Stone-dwelling actinobacteria Blastococcus saxobsidens, Modestobacter marinus and Geodermatophilus obscurus proteogenomes. The ISME Journal. doi: 10.1038/ismej.2015.108.

  • Svistoonoff S, et al. 2015. How Transcriptomics Revealed New Information on Actinorhizal Symbioses Establishment and Evolution. Biological Nitrogen Fixation, 2 Volume Set. 425.


  • Berry AM, Barabote RD, Normand P. 2014. The Family Acidothermaceae. In: The Prokaryotes. Acosta-Cruz, E, DeLong, EF, Lory, S, Stackebrandt, E, & Thompson, F. Springer Berlin Heidelberg: Berlin, Heidelberg p. 13-19.

  • Cotin-Galvan L. 2014. Relation plante-hôte / Frankia dans les symbioses actinorhiziennes : cas particulier des souches non-isolables capables de sporuler in-planta. (Accessed no date).

  • Nouioui I. 2014. Phylogénie et évolution du genre Frankia. (Accessed no date).

  • Nouioui I, et al. 2014. Absence of Cospeciation between the Uncultured Frankia Microsymbionts and the Disjunct Actinorhizal Coriaria Species. BioMed Research International. 2014:1-9. doi: 10.1155/2014/924235.

  • Pozzi AC. 2014. Rôles adaptatifs et contraintes de la sporulation chez les microorganismes associés aux plantes : cas de la sporulation in planta dans la symbiose actinorhizienne Frankia (Frankiaceae)–Alnus (Betulaceae). Lyon 1

  • Normand P, Benson DR, Berry AM, Tisa LS. 2014. The Family Frankiaceae. In: The Prokaryotes. Rosenberg, E, DeLong, EF, Lory, S, Stackebrandt, E, & Thompson, F. Springer Berlin Heidelberg: Berlin, Heidelberg p. 339-356.

  • Normand P, Daffonchio D, Gtari M. 2014. The Family Geodermatophilaceae. In: The Prokaryotes. Rosenberg, E, DeLong, EF, Lory, S, Stackebrandt, E, & Thompson, F. Springer Berlin Heidelberg: Berlin, Heidelberg p. 361-379.

  • Sen A, et al. 2014. The phylogeny of actinobacteria revisited in the light of complete genomes, the orders Frankiales and Micrococcales should be split into coherent entities. Proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. International Journal of Systematic and Evolutionary Microbiology. ijs.0.063966-0. doi: 10.1099/ijs.0.063966-0.

  • Toussirot M, et al. 2014. Dyeing properties, coloring compounds and antioxidant activity of Hubera nitidissima (Dunal) Chaowasku (Annonaceae). Dyes and Pigments. 278-284. doi: 10.1016/j.dyepig.2013.11.010.