Philippe Normand

Claude Bernard University Lyon 1 | UCBL

Uptake hydrogenase (Hup) recycles H2 formed by nitrogenase during nitrogen fixation, thereby preserving energy. Among root nodule bacteria, most rhizobial strains examined are Hup−, while only one Hup− Frankia inoculum had been identified. Previous analyses had led to the identification of two different [NiFe] hydrogenase syntons. We analysed the d...

Non-specific lipid transfer proteins (nsLTPs) are antimicrobial peptides, involved in several plant biological processes including root nodule nitrogen fixation (RNF). Nodulating plants belonging to the RNF clade establish symbiosis with the nitrogen-fixing bacteria rhizobia (legumes symbiosis model) and Frankia (actinorhizal symbiosis model) leadi...

Frankia strain Ag45/Mut15T was isolated from a root nodule of Alnus glutinosa growing in a swamp at lake Grossensee, Germany. The strain forms root nodules on A. glutinosa, in which it produces hyphae and clusters of N2-fixing vesicles. N2-fixing vesicles are also produced in nitrogen-free growth medium, in addition to hyphae and sporangia. The who...

A phyloprofile of Frankia genomes was carried out to identify those genes present in symbiotic strains of clusters 1, 1c, 2 and 3 and absent in non-infective strains of cluster 4. At a threshold of 50% AA identity, 108 genes were retrieved. Among these were known symbiosis-associated genes such as nif (nitrogenase), and genes which are not know as...

The genomes of two nitrogen-fixing Frankia strains, AiPa1 and AiPs1, are described as representatives of two novel candidate species. Both strains were isolated from root nodules of Alnus incana, used as capture plants in bioassays on soils from a reforested site at Karttula, Finland, that was devoid of actinorhizal plants but contained 25 year-old...

The authors wish to make the following corrections to this paper [...]

The Frankia sp. strain R82 genome is described as representative of a novel candidate species within Frankia cluster 1, as indicated by average nucleotide identity (ANI) analyses, with its closest relatives being Frankia nodulisporulans AgTrs and strains Ag45/Mut15 and AgPM24 (86% identity).

Frankia spp. are nitrogen-fixing actinobacteria that establish root-nodule symbiosis with actinorhizal plants comprising more than 200 species in eight dicotyledonous families. From a cell population of Frankia alni strain ACN14a that had been subcultured for over 30 years, we identified two types of variants (types A and S) with a different colony...

Background Cadmium (Cd²⁺) is one of the highly toxic heavy metals and is considered as a carcinogenic agent. Our aim was to confirm Frankia alni ACN14a ability to resist Cd²⁺ and determine the genes involved in the resistance. Results Up to 10 and 22 times in Cd²⁺ accumulation were detected in F. alni ACN14a and Frankia casuarinae CcI3 hyphae when...

The response of Alnus glutinosa to Frankia alni ACN14a is driven by several sequential physiological events from calcium spiking and root-hair deformation to the development of the nodule. Early stages of actinorhizal symbiosis were monitored at the transcriptional level to observe plant host responses to Frankia alni. Forty-two genes were signific...

The genomes of two nitrogen-fixing Frankia strains, AgB32 and AgKG'84/4, were isolated from spore-containing (spore+) and spore-free (spore-) root nodules of Alnus glutinosa, but they did not sporulate upon reinfection. The two strains are described as representatives of two novel candidate species. Phylogenomic and ANI analyses indicate that each...

Two bacteria belonging to the Pseudomonas and Pantoea genera were isolated from olive knots. Both bacterial strains were omnipresent in this study’s olive orchard with high susceptibility of the autochthonous olive genotypes indicating coevolution of bacteria with host plants. Genomes of two endemic bacteria show conserved core genomes and genome p...

The genomes of two nitrogen-fixing Frankia strains, Ag45/Mut15 and AgPM24, isolated from root nodules of Alnus glutinosa are described as representatives of a novel candidate species. Phylogenomic and ANI analyses confirmed that both strains are related to cluster 1 frankiae, and that both strains belong to a novel species. At 6.4 - 6.7 Mb, their g...

Omics are the most promising approaches to investigate microbes for which no genetic tools exist such as the nitrogen-fixing symbiotic Frankia. A proteogenomic analysis of symbiotic Frankia alni was done by comparing those proteins more and less abundant in Alnus glutinosa nodules relative to N2-fixing pure cultures with propionate as the carbon so...

In the present study, an analysis of antimicrobial activity; and an assessment of genomic biocontrol attributes of the recently described radioresistant strain Kocuria rhizophila PT10 were conducted. PT10, a Gram-positive and yellow pigmented actinobacterial strain, was isolated from the roots of xerophyte Panicum turgidum collected from Ksar Ghila...

The response of Alnus glutinosa to Frankia alni is complex with several sequential physiological modifications that include calcium spiking, root hair deformation, penetration, induction of primordium, formation and growth of nodule. A transcriptomic study of seedlings in hydroponics after early contact (2.5 days) with Frankia alni , either with a...

Bacterial communities associated with roots of Panicum turgidum, exposed to arid conditions, were investigated with a combination of cultural and metataxonomic approaches. Traditional culture-based techniques were used and 32 isolates from the irradiated roots were identified as belonging to Actinobacteria, Bacteroidetes, Firmicutes and Proteobacte...

A new strain belonging to the genus Kocuria, designed PT10, was isolated from irradiated roots of the xerophyte Panicum turgidum. Isolate PT10 is a Gram-positive, coccoid, aerobic and ionizing-radiation (IR)-resistant actinobacterium. PT10 has shown an ability to survive under extreme conditions, such as gamma irradiation, desiccation and high conc...

We describe a new Frankia species, for three non-isolated strains obtained from Alnus glutinosa in France and Sweden, respectively. These strains can nodulate several Alnus species (A. glutinosa, A. incana, A. alnobetula), they form hyphae, vesicles and sporangia in the root nodule cortex but have resisted all attempts at isolation in pure culture....

The members of the genus Frankia are, with a few exceptions, a group of nitrogen-fixing symbiotic actinobacteria that nodulate mostly woody dicotyledonous plants belonging to three orders, eight families and 23 genera of pioneer dicots. These bacteria have been characterized phylogenetically and grouped into four molecular clusters. One of the clus...

A.ci.do.ther'mus. L. masc. adj. acidus sour, acid; Gr. masc. adj. thermus hot; N.L. masc. n. Acidothermus acid and hot (loving). Actinobacteria / Actinobacteria / Acidothermales / Acidothermaceae / Acidothermus The genus Acidothermus contains a single species, Acidothermus cellulolyticus, isolated from a thermal spring, consisting of rods and filam...

A.ci.do.ther.ma.ce'ae. N.L. masc. n. Acidothermus type genus of the family; suff. ‐aceae ending to denote a family; N.L. fem. pl. n. Acidothermaceae the Acidothermus family. Actinobacteria / Actinobacteria / Acidothermales / Acidothermaceae A one‐genus family, alone in the order Acidothermales, containing thermophilic, acidophilic, and cellulolytic...

Fran.ki.a'les. N.L. fem. n. Frankia type genus of the order; suff. ‐ ales ending to denote an order; N.L. fem. pl. n. Frankiales the Frankia order. Actinobacteria / Actinobacteria / Frankiales A group of slow‐growing aerobic to microaerophilic soil‐inhabiting mesophilic, mostly nitrogen‐fixing, organisms in symbiosis with pioneer plants. Some linea...

Fran.ki.a.ce'ae. N.L. fem. n. Frankia type genus of the family; suff. ‐ aceae ending to denote a family; N.L. fem. pl. n. Frankiaceae the Frankia family. Actinobacteria / Actinobacteria / Frankiales / Frankiaceae A group of slow‐growing aerobic to microaerophilic soil‐inhabiting mesophilic, mostly nitrogen‐fixing, organisms in symbiosis with pionee...

A.ci.do.ther.ma'les. N.L. masc. n. Acidothermus type genus of the order; suff. ‐ales ending to denote an order; N.L. fem. pl. n. Acidothermales the Acidothermus order. Actinobacteria / Actinobacteria / Acidothermales A one family, one genus order containing thermophilic, acidophilic, and cellulolytic bacteria that inhabit hot springs. Their phyloge...

Symbiosis established between actinorhizal plants and Frankia spp., which are nitrogen-fixing actinobacteria, promotes nodule organogenesis, the site of metabolic exchange. The present study aimed to identify amino acid markers involved in Frankia-Alnus interactions by comparing nodules and associated roots from field and greenhouse samples. Our re...

Fran.ki.a. N.L. fem. n. Frankia named after Albert Bernhard Frank (1839–1900), a Swiss plant biologist, who studied extensively nitrogen nutrition in legumes and the microorganisms causing root nodulation from 1877 to 1892 and who coined the term “symbiosis.” Actinobacteria / Actinobacteria / Frankiales / Frankiaceae / Frankia A group of soil‐inhab...

We report the genome sequence of a Pseudomonas sp. strain isolated from olive knot galls. The genome size is 6.101 Mbp with a G+C content of 58%. A total of 6,137 coding DNA sequences (CDS) were predicted, including 52 tRNA and 4 rRNA genes.

Here, we present the total genome sequence of Pantoea sp. strain paga, a plant-associated bacterium isolated from knots present on olive trees grown on the Adriatic Coast. The genome size of Pantoea sp. paga is 5.08 Mb, with a G+C content of 54%. The genome contains 4,776 predicted coding DNA sequences (CDSs), including 70 tRNA genes and 1 ribosoma...

Actinobacteria from genus Frankia are able to form symbiotic associations with actinorhizal plants including alders. Among them, Sp+ strains are characterized by their ability to differentiate numerous sporangia inside host plant cells (unlike "Sp-" strains unable of in-planta sporulation). Here, we report the first genome sequences of three unisol...

The taxonomic assignment of uncultured prokaryotes to known taxa is a major challenge in microbial systematics. This relies usually on the phylogenetic analysis of the ribosomal small subunit RNA or a few housekeeping genes. Recent works have disclosed ribosomal proteins as valuable markers for systematics and, due to the boom in complete genome se...

Spor.ich'thy.a. Gr. fem. n. spora seed (and in biology, a spore); Gr. masc. n. ichthys fish; N.L. fem. n. Sporichthya an organism with fish‐like spores. Actinobacteria / Actinobacteria / Frankiales / Sporichthyaceae / Sporichthya Aerobic or facultatively anaerobic actinobacteria. Cells are Gram‐stain‐variable, with young cells being Gram‐stain‐nega...

Spor.ich.thy.a'les. (N.L. fem. n. Sporichthya, type genus of the order; ‐ales, ending to denote an order; N.L. fem. pl. n. Sporichthyales, the Sporichthya order). Actinobacteria / Actinobacteria / Sporichthyales Soil‐inhabiting actinobacteria with a unique morphology. Short aerial mycelium forms rod‐shaped to coccoid spores that may develop polar f...

Spo.ro.tri.cha.ce'ae. N.L. fem. n. Sporichthya type genus of the family; suff. ‐aceae ending to denote a family; N.L. fem. pl. n. Sporichthyaceae the Sporichthya family. Actinobacteria / Actinobacteria / Frankiales / Sporichthyaceae Group of microorganisms with a unique and complex morphology. Aerobic or facultatively anaerobic. Gram‐stain‐variable...

Sporulation is a microbial adaptive strategy to resist inhospitable conditions for vegetative growth and to disperse to colonise more favourable environments. This microbial trait is widespread in Actinobacteria. Among them, Frankia strains are able to differentiate sporangia in pure culture, while others can sporulate even when in symbiosis with s...

The purpose of this study was to explore the microbial potential of a semi-arid sandy soil from south-central Algeria in order to isolate new chitinolytic actinobacteria. This soil is subjected to high temperatures (up to 43 °C) and has low nutrient content. Strains were isolated by plating soil suspensions on Bennett and Colloidal Chitin (CCM) med...

Natural products are a rich source of potential drugs for many applications. Discovery of natural products through the activation of cryptic gene clusters encoding their biosynthetic pathways, engineering of those biosynthetic pathways and optimization of production yields often rely on the expression of these gene clusters in suitable heterologous...

Strain ARgP5T, an actinobacterium isolated from a root nodule present on an Alnus incana subspecies rugosa shrub growing in Quebec City, Canada, was the subject of polyphasic taxonomic studies to clarify its status within the genus Frankia . 16S rRNA gene sequence similarities and ANI values between ARgP5T and type strains of species of the genus F...

The type isolates of species Micromonospora saelicesensis and Micromonospora noduli are Gram-stain positive actinobacteria that were originally isolated from nitrogen fixing nodules of the legumes Lupinus angustifolius and Pisum sativum, respectively. These two species are very closely related and questions arise as to whether they should be merged...

Number of orthologous genes that conform the pan genome, core genome and singletons of Micromonospora saelicesensis (Group 1) and Micromonospora noduli (Group II). In parenthesis, values expressed as percentages based on an average genome of 6531 genes for M. saelicesensis and 6540 genes for M. noduli.

Pair-wise OGRI values for ANI, OrthoANI and dDDH between M. saelicesensis (Group I) and M. noduli (Group II) strains.

List of genes used in core-genome phylogenomic analysis based on UBCG (Na et al., 2018).

(A) Venn diagram showing the number of orthologous genes clusters that integrate the core and disposable genomes, and singletons of all strains in Group I (Micromonospora saelicesensis). (B) Venn diagram showing the number of orthologous gene clusters that integrate the core genome and disposable genomes, and singletons of all strains in Group II (...

Pan- and Core genome development plot of Micromonospora noduli and Micromonospora saelicesensis strains. The orange and blue lines show the progression in the pan- and core genomes as more genomes are added.

Predicted phenotypes vs. experimental phenotypic data based on 19 carbon source substrates. In silico prediction negative, phenotype not expressed (purple); in silico prediction negative (genes not found), phenotype expressed (red); in silico prediction positive, phenotype not expressed (light green) and in silico prediction positive, phenotype exp...

Genome sequence accession numbers of strains used in this work.

BIOLOG phenotypic profiles of M. saelicesensis and M. noduli strains. +, positive; –, negative; c, conflicting.

Differential phenotypic characteristics between M. saelicesensis and M. noduli as reported by Carro and colleagues (Carro et al., 2016). +, Positive; –, Negative; w, Weak.

Carbon source substrates tested at different times using the same laboratory conditions. +, positive; –, negative; w, weak.

Genomic traces of symbiosis loss A symbiosis between certain bacteria and their plant hosts delivers fixed nitrogen to the plants. Griesmann et al. sequenced several plant genomes to analyze why nitrogen-fixing symbiosis is irregularly scattered through the evolutionary tree (see the Perspective by Nagy). Various genomes carried traces of lost path...

Diazotrophic Actinobacteria of the genus Frankia represent a challenge to classical bacterial taxonomy as they include many unculturable strains. As a consequence, we still have a poor understanding of their diversity, evolution and biogeography. In this study, a Multi-Locus Sequence Analysis (MLSA) using atpD, dnaA, ftsZ, pgk, and rpoB loci was do...

Actinorhizal plants are ecologically and economically important. Symbiosis with nitrogen-fixing bacteria allows these woody dicotyledonous plants to colonise soils under nitrogen deficiency, water-stress or other extreme conditions. However, proteins involved in xerotolerance of symbiotic microorganisms have yet to be identified. Here we characteri...

How can the evolutionary success of prokaryotes be explained ? How did they manage to survive conditions that have fluctuated, with drastic events over 3.5 billion years ? Which significant metabolisms and mechanisms have appeared over the course of evolution that have permitted them to survive the most inhospitable conditions from the physicochemi...

The various schemes proposed to classify microorganisms in the living world have long been subject of heated debates. The classical dichotomic distinction between Prokaryotae (cells without nucleus) and Eukaryotae (cells with nucleus) functional and phenotypic categories was deeply changed by rRNA gene-based analysis that divided the living world i...

Evolution is a phenomenon that escapes immediate attention because changes occur at a very slow pace and are often considered at odds with a religious vision of the world. Using bacteria that replicate so much faster than eukaryotes has permitted to quantify and discern tendencies. Such laboratory evolution implies growth rate, ability to use this...

How can the evolutionary success of prokaryotes be explained? How did they manage to survive conditions that have fluctuated, with drastic events over 3.5 billion years? Which significant metabolisms and mechanisms have appeared over the course of evolution that have permitted them to survive the most inhospitable conditions from the physicochemica...

Creating a hierarchical system for microbes began as soon as microbes were discovered and has been constantly evolving ever since. The larger categories, the techniques to define taxa, and the bibliographical conventions, all these are regularly changing. At the moment, there are 30 bacterial phyla and 6 archaeal phyla that are described. The impac...

The purpose of this book is to show the essential and indispensable role of prokaryotes in the evolution of a living world. The evolutionary success of prokaryotes is explained together with their role in the evolution of the geosphere, the biosphere and its functioning, as well as their ability to colonize all biotopes, including the most extreme...

The various schemes proposed to classify microorganisms in the living world have long been subject of heated debates. The classical dichotomic distinction between Prokaryotae (cells without nucleus) and Eukaryotae (cells with nucleus) functional and phenotypic categories was deeply changed by rRNA gene-based analysis that divided the living world i...

How can the evolutionary success of prokaryotes be explained ? How did they manage to survive conditions that have fluctuated, with drastic events over 3.5 billion years ? Which significant metabolisms and mechanisms have appeared over the course of evolution that have permitted them to survive the most inhospitable conditions from the physicochemi...

The various schemes proposed to classify microorganisms in the living world have long been subject of heated debates. The classical dichotomic distinction between Prokaryotae (cells without nucleus) and Eukaryotae (cells with nucleus) functional and phenotypic categories was deeply changed by rRNA gene-based analysis that divided the living world i...

The genus Frankia comprises a group of nitrogen-fixing actinobacteria that form root-nodule symbioses with perennial dicotyledonous plants in the nitrogen-fixing clade. These bacteria have been characterized phylogenetically and grouped into four clusters (clusters 1-4). Cluster 2 contains mostly uncultured strains that induce nodules on species of...

Before the establishment of pure cultures, the species Frankia alni, ‘Frankia casuarinae’ and ‘Frankia elaeagni’ were proposed to encompass all causal agents of the nitrogen-fixing root nodules of dicotyledonous plants from the genera Alnus, Casuarina or Elaeagnus. The sole Frankia species with a validly published name, the type species F. alni, wa...

To gain more insight in nitrogen metabolism in actinorhizal nodules, a comparison between the N metabolite profiles in roots vs. nodules was initiated for one host plant from the best-examined order of actinorhizal plants, Fagales, A. glutinosa (Betulaceae), a temperate tree, and one host plant from the Cucurbitales order, Datisca glomerata (Datisc...

Functional domains are semi-autonomous parts of proteins. The Per-Arnt-Sim (PAS) domain functions as signal-sensor in two-component systems of several bacteria. This domain exhibits large sequence diversity and is linked to other co-domains to modulate their function. In the present study, we analyzed the PAS domains found in the proteomes of sever...

Frankia sp. strain G2 was originally isolated from Casuarina equisetifolia and is characterized by its ability to nodulate actinorhizal plants of the Rhamnales order, but not its original host. It represents one of the largest Frankia genomes so far sequenced (9.5 Mbp).

Alnus glutinosa has been shown previously to synthesize, in response to nodulation by Frankia sp. ACN14a, an array of peptides called Alnus symbiotic up-regulated peptides (ASUP). In a previous study one peptide (Ag5) was shown to bind to Frankia nitrogen-fixing vesicles and to modify their porosity. Here we analyse 4 other ASUPs, alongside Ag5, to...

The Geodermatophilaceae are unique model systems to study the ability to thrive on or within stones and their proteogenomes (referring to the whole protein arsenal encoded by the genome) could provide important insight into their adaptation mechanisms. Here we report the detailed comparative genome analysis of Blastococcus saxobsidens (Bs), Modesto...

Frankia strain R43 is a nitrogen-fixing and hydrogen-producing symbiotic actinobacterium that was isolated from nodules of Casuarina cunninghamiana but infects only Elaeagnaceae . This communication reports the genome of the strain R43 and provides insights into the microbe genomics and physiological potentials.

Frankia strain R43 is a nitrogen-fixing and hydrogen-producing symbiotic actinobacterium that was isolated from nodules of Casuarina cunninghamiana but infects only Elaeagnaceae. This communication reports the genome of the strain R43 and provides insights into the microbe genomics and physiological potentials.

Microbes are phylogenetically (Archaea, Bacteria, Eukarya, and viruses) and functionally diverse. They colonize highly varied environments and rapidly respond to and evolve as a response to local and global environmental changes, including those induced by pollutants resulting from human activities. This review exemplifies the Microbial Ecology EC2...

At present, there are six published genomes of the actinobacterium Frankia with six more at various stages of completion and several more are being planned. These genomes cover the four known phylogenetic clusters and range in size from five to ten Mb. The strains studied have different symbiotic status ranging from obligate symbionts to non-symbio...

Fran.ki.a.ce'a.e. N.L. fem. n. Frankia type genus of the family; suff. -aceae ending to denote a family; N.L. fem. pl. n. Frankiaceae the Frankia family. Actinobacteria / Actinobacteria / Frankiales / Frankiaceae

Qua.dri.spha'e.ra. L. pref. numer. adj. quadr ‐ four; L. fem. n. sphaera a ball, a globe, a sphere; N.L. fem. n. Quadrisphaera fourfold balls, coccus in tetrad. Actinobacteria / Actinobacteria / Kineosporiales / Kineosporiaceae / Quadrisphaera Gram‐positive, non‐spore‐forming cocci, 1.2–3.0 µm in diameter, occurring in tetrad arrangements (Figure 1...

Ki.ne.o.spo.ri.a.ce'a.e. N.L. fem. n. Kineosporia type genus of the family; suff. -aceae ending to denote a family; N.L. fem. pl. n. Kineosporiaceae the Kineosporia family. Actinobacteria / Actinobacteria / Kineosporiales / Kineosporiaceae