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Equipe de Recherche Groupes fonctionnels du cycle de l’azote

Feth-el-Zahar Haichar

Maître de conférences


  • Thèmes de recherches :
    1. Eco-physiologie des bactéries dénitrifiantes
    2. Regulation de la dénitrification dans la rhizosphère
    3. Interaction plant-bactérie dans la rhizosphère (diversité et fonctionnement)

Parcours scientifique

  • MCF depuis Sep 2010 à l’université Lyon 1, au LEM
  • Etude post doctoral de 2008-2010 au DMF, Lausanne, Suisse
  • Docteur en Microbiologie moléculaire et Biotechnologie de l’université Aix-Marseille II en 2008, Laboratoire LEMiRE, cea Cadarache





  • Bardon C, et al. 2017. Biological denitrification inhibition (BDI) with procyanidins induces modification of root traits, growth and N status in Fallopia x bohemica. Soil Biology and Biochemistry. 107:41-49. doi: 10.1016/j.soilbio.2016.12.009.
    Résumé : Nitrogen (N) limits plant growth in many ecosystems and denitrification is a major source of N loss from soils. Fallopia spp. is an invasive plant species complex adapted to low-fertility soils, which is responsible for biological denitrification inhibition (BDI) through the production of procyanidins. However, the extent to which procyanidins can affect Fallopia spp. via BDI has not yet been shown. We investigated how procyanidins can generate plant trait modifications in Fallopia x bohemica by adding them, or not, to soil mesocosms planted, or not, with F. x bohemica. Soil denitrification enzyme activity (DEA), soil substrate induced respiration (SIR), nitrification enzyme activity (NEA), N-mineralization and total N, and NO3− concentrations were measured in the soil of planted mesocosms. NO3− concentrations were measured in unplanted mesocosms. Leaf and root N contents and above- and belowground plant traits were measured. In unplanted soils, procyanidins induced a six-fold increase in NO3−. Procyanidins inhibited DEA but not SIR, NEA and N-mineralization in planted soil. Procyanidins increased root N content marginally and biomass allocation to roots, while modifying root traits associated with an increase in nutrient acquisition capacity. Our results suggest that a plant-soil feedback related to BDI could result from procyanidin production in Fallopia spp..
    Mots-clés : #5, #cesn, Biological denitrification inhibition, Fallopia spp., Nitrate, Plant trait modifications, Procyanidins, Root/shoot ratio.

  • Guyonnet JP, et al. 2017. The effects of plant nutritional strategy on soil microbial denitrification activity through rhizosphere primary metabolites. FEMS Microbiology Ecology. 93. doi: 10.1093/femsec/fix022.
    Mots-clés : #3, #5.


  • Bardon C, et al. 2016. Mechanism of biological denitrification inhibition (BDI): procyanidins induce an allosteric transition of the membrane-bound NO3-reductase through membrane alteration. FEMS Microbiology Ecology. fiw034. doi: 10.1093/femsec/fiw034.
    Résumé : Recently, it has been shown that procyanidins from Fallopia spp. inhibit bacterial denitrification, a phenomenon called biological denitrification inhibition (BDI). However, the mechanisms involved in such a process remain unknown. Here, we investigate the mechanisms of BDI involving procyanidins, using the model strain Pseudomonas brassicacearum NFM 421.The aerobic and anaerobic (denitrification) respiration, cell permeability and cell viability of P. brassicacearum were determined as a function of procyanidin concentration. The effect of procyanidins on the bacterial membrane was observed using transmission electronic microscopy (TEM). Bacterial growth, denitrification, NO3- and NO2-reductase activity, the expression of sub-units of NO3- (narG) and the NO2-reductase (nirS) under NO3 or NO2 were measured with and without procyanidins.Procyanidins inhibited the denitrification process without affecting aerobic respiration at low concentrations. Procyanidins also disturbed cell membranes without affecting cell viability. They specifically inhibited NO3- but not NO2-reductase. P. brassicacearum responded to procyanidins by over-expression of the membrane-bound NO3-reductase sub-unit (narG).Our results suggest that procyanidins can specifically inhibit membrane-bound NO3-reductase inducing enzymatic conformational changes through membrane disturbance and that P. brassicacearum responds by over-expressing membrane-bound NO3-reductase. Our results lead the way to a better understanding of BDI.
    Mots-clés : #5, Allosteric transition, biological denitrification inhibition, membrane alteration, membrane-bound enzyme, nitrate-reductase, procyanidins.

  • Haichar FZ, Heulin T, Guyonnet JP, Achouak W. 2016. Stable isotope probing of carbon flow in the plant holobiont. Current Opinion in Biotechnology. 41:9-13. doi: 10.1016/j.copbio.2016.02.023.
    Résumé : Microbial communities associated with a plant host, constituting a holobiont, affect the physiology and growth of the plant via metabolites that are mainly derived from their photosynthates. The structure and function of active microbial communities that assimilate root exudates can be tracked by using stable isotope probing (SIP) approaches. This article reviews results from ongoing SIP research in plant–microbe interactions, with a specific focus on investigating the fate of fresh and recalcitrant carbon in the rhizosphere with 13C enriched-root exudates, in addition to identifying key players in carbon cycling. Finally, we discuss new SIP applications that have the potential to identify novel enzymes implicated in rhizoremediation or plant genes dedicated to root exudation by combining SIP approaches and genome wide associations studies.
    Mots-clés : #5.


  • Bardon C, et al. 2015. Identification of B-type procyanidins in <i>Fallopia</i> spp. involved in biological denitrification inhibition (BDI): B-type procyanidins from Fallopia involved in BDI. Environmental Microbiology. doi: 10.1111/1462-2920.13062.
    Mots-clés : #3, #5, #cesn.

  • Faure D, et al. 2015. Environmental microbiology as a mosaic of explored ecosystems and issues. Environmental Science and Pollution Research International. 22:13577-13598. doi: 10.1007/s11356-015-5164-5.
    Résumé : 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 EC2CO consortium's efforts to explore the biology, ecology, diversity, and roles of microbes in aquatic and continental ecosystems.
    Mots-clés : #5.

  • Harfouche L, Haichar FZ, Achouak W. 2015. Small regulatory RNAs and the fine-tuning of plant–bacteria interactions. New Phytologist. doi: 10.1111/nph.13195.
    Résumé : Small regulatory RNAs (sRNAs) play a key role in many physiological and adaptive responses in bacteria. Faced with rapidly changing environments, it is more advantageous for bacteria to use sRNA-mediated responses than regulation by protein transcriptional factors, as sRNAs act at the post-transcriptional level and require less energy and time for their synthesis and turnover. The use of RNA deep sequencing has provided hundreds of sRNA candidates in different bacterial species that interact with plants. Here, we review the most recent results for the involvement of bacterial sRNAs in beneficial as well as deleterious plant–bacteria interactions. We describe the current view for the role of sRNAs, which are suggested to improve competition for both niches and resources in plant-interacting bacteria. These sRNAs also help plant-associated bacteria individually adapt to the rapidly changing conditions to which they are exposed, during different stages of this interaction.
    Mots-clés : #5, beneficial bacteria, pathogenic bacteria, plant–bacteria interactions, regulation, small regulatory RNAs (sRNAs).


  • Bardon C, et al. 2014. Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytologist. 204:620-630. doi: 10.1111/nph.12944.
    Résumé : * Previous studies on the effect of secondary metabolites on the functioning of rhizosphere microbial communities have often focused on aspects of the nitrogen (N) cycle but have overlooked biological denitrification inhibition (BDI), which can affect plant N-nutrition. Here, we investigated the BDI by the compounds of Fallopia spp., an invasive weed shown to be associated with a low potential denitrification of the soil. * Fallopia spp. extracts were characterized by chromatographic analysis and were used to test the BDI effects on the metabolic and respiratory activities of denitrifying bacteria, under aerobic and anaerobic (denitrification) conditions. The BDI of Fallopia spp. extracts was tested on a complex soil community by measuring denitrification enzyme activity (DEA), substrate induced respiration (SIR), as well as abundances of denitrifiers and total bacteria. * In 15 strains of denitrifying bacteria, extracts led to a greater BDI (92%) than respiration inhibition (50%). Anaerobic metabolic activity reduction was correlated with catechin concentrations and the BDI was dose dependent. In soil, extracts reduced the DEA/SIR ratio without affecting the denitrifiers: total bacteria ratio. * We show that secondary metabolite(s) from Fallopia spp. inhibit denitrification. This provides new insight into plant–soil interactions and improves our understanding of a plant's ability to shape microbial soil functioning.
    Mots-clés : #3, #5, #cesn, biological inhibition, catechin derivates, Denitrification, Fallopia spp., nitrogen cycle, rhizosphere, secondary metabolites, weeds.

  • Haichar FZ, Santaella C, Heulin T, Achouak W. 2014. Root exudates mediated interactions belowground. Soil Biology and Biochemistry. 77:69-80. doi: 10.1016/j.soilbio.2014.06.017.
    Résumé : The root exudate composition reflects the contradictory-concomitantly attractive and repulsive-behaviour of plants towards soil microorganisms. Plants produce antimicrobial, insecticide and nematicide compounds to repel pathogens and invaders. They also produce border cells that detach from roots and play an important role as biological and physical barrier against aggressors. Plants produce also metabolites used as carbon source resulting in the attraction of phytobeneficial soil microorganisms that help plants in controlling diseases directly via the production of antimicrobial compounds or indirectly via the induction of plant systemic resistance. The root exudates may have a direct impact on carbon and nitrogen cycling, as they exhibit a rhizosphere priming effect towards soil organic matter degraders, and may inhibit nitrification process by soil nitrifying microorganisms. They also contain signalling molecules required for the establishment of ‘plant-microorganisms’ interactions. The composition of root exudates is therefore broad ranging, consisting of feeding, antimicrobial and signalling molecules. We thus focused this review on current research concerning the role of the root exudate composition in ‘plant-microorganisms’ interactions and functioning of the rhizosphere.
    Mots-clés : #5, Chemotaxis, Defence, Nutrients, Plant–microbe interactions, Signalling molecules, symbiosis.


  • Haichar FZ, Fochesato S, Achouak W. 2013. Host Plant Specific Control of 2,4-Diacetylphloroglucinol Production in the Rhizosphere. Agronomy. 3:621-631. doi: 10.3390/agronomy3040621.
    Mots-clés : #5.


  • Haichar FZ, Roncato MA, Achouak W. 2012. Stable isotope probing of bacterial community structure and gene expression in the rhizosphere of <i>Arabidopsis thaliana</i>. FEMS Microbiology Ecology. 81:291–302. doi: 10.1111/j.1574-6941.2012.01345.x.
    Résumé : The rhizosphere is an active compartment where plant and microorganisms establish a molecular dialogue. In this study, we analysed the impact of Arabidopsis thaliana on bacterial community structure and the expression of certain beneficial genes using DNA- and mRNA-SIP in the rhizosphere of plantlets grown under 13CO2 for 13, 21 and 27 days. DNA- and rRNA-SIP revealed changes in bacterial communities inhabiting the rhizosphere soil that were probably related to modification of root exudates, while root-colonizing populations were maintained over time suggesting their metabolic versatility and adaptation. The impact of the plant via root exudates on the expression of the noncoding RNAs rsmZ,acdS gene encoding 1-aminocyclopropane-1-carboxylate deaminase and nosZ gene encoding nitrous oxide reductase, in the root-adhering soil and on the roots of A. thaliana was determined using mRNA-SIP. Results showed that these genes were present and expressed by bacteria inhabiting roots and by those that derive nutrients from the breakdown of organic matter in soils or from root exudates. The expression of rsmZ under natural conditions indicates the importance of noncoding RNAs in bacterial adaptation to their ecological niches.
    Mots-clés : #5, gene expression, microbial community structure, mRNA-SIP, rhizosphere.

  • Sonnleitner E, et al. 2012. Novel Targets of the CbrAB/Crc Carbon Catabolite Control System Revealed by Transcript Abundance in <i>Pseudomonas aeruginosa</i>. PLoS ONE. 7:e44637. doi: 10.1371/journal.pone.0044637.
    Résumé : The opportunistic human pathogen Pseudomonas aeruginosa is able to utilize a wide range of carbon and nitrogen compounds, allowing it to grow in vastly different environments. The uptake and catabolism of growth substrates are organized hierarchically by a mechanism termed catabolite repression control (Crc) whereby the Crc protein establishes translational repression of target mRNAs at CA (catabolite activity) motifs present in target mRNAs near ribosome binding sites. Poor carbon sources lead to activation of the CbrAB two-component system, which induces transcription of the small RNA (sRNA) CrcZ. This sRNA relieves Crc-mediated repression of target mRNAs. In this study, we have identified novel targets of the CbrAB/Crc system in P. aeruginosa using transcriptome analysis in combination with a search for CA motifs. We characterized four target genes involved in the uptake and utilization of less preferred carbon sources: estA (secreted esterase), acsA (acetyl-CoA synthetase), bkdR (regulator of branched-chain amino acid catabolism) and aroP2 (aromatic amino acid uptake protein). Evidence for regulation by CbrAB, CrcZ and Crc was obtained in vivo using appropriate reporter fusions, in which mutation of the CA motif resulted in loss of catabolite repression. CbrB and CrcZ were important for growth of P. aeruginosa in cystic fibrosis (CF) sputum medium, suggesting that the CbrAB/Crc system may act as an important regulator during chronic infection of the CF lung.
    Mots-clés : #5.


  • Bressan M, et al. 2009. Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. The ISME Journal. 3:1243-1257. doi: 10.1038/ismej.2009.68.
    Résumé : A specificity of Brassicaceous plants is the production of sulphur secondary metabolites called glucosinolates that can be hydrolysed into glucose and biocidal products. Among them, isothiocyanates are toxic to a wide range of microorganisms and particularly soil-borne pathogens. The aim of this study was to investigate the role of glucosinolates and their breakdown products as a factor of selection on rhizosphere microbial community associated with living Brassicaceae. We used a DNA-stable isotope probing approach to focus on the active microbial populations involved in root exudates degradation in rhizosphere. A transgenic Arabidopsis thaliana line producing an exogenous glucosinolate and the associated wild-type plant associated were grown under an enriched 13CO2 atmosphere in natural soil. DNA from the rhizospheric soil was separated by density gradient centrifugation. Bacterial (Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Acidobacteria), Archaea and fungal community structures were analysed by DGGE fingerprints of amplified 16S and 18S rRNA gene sequences. Specific populations were characterized by sequencing DGGE fragments. Roots of the transgenic plant line presented an altered profile of glucosinolates and other minor additional modifications. These modifications significantly influenced microbial community on roots and active populations in the rhizosphere. Alphaproteobacteria, particularly Rhizobiaceae, and fungal communities were mainly impacted by these Brassicaceous metabolites, in both structure and composition. Our results showed that even a minor modification in plant root could have important repercussions for soil microbial communities.
    Mots-clés : #3, #cesn, Arabidopsis thaliana, DNA-SIP, fungi, isothiocyanate, rhizobia, rhizosphere.


  • Darcheville O, et al. 2008. Aqueous, solid and gaseous partitioning of selenium in an oxic sandy soil under different microbiological states. Journal of environmental radioactivity. 99:981-992. doi: 10.1016/j.jenvrad.2007.11.006.
    Résumé : The aim of this study was to investigate the role of microorganisms on the behaviour of selenium in natural soil maintained under strictly aerobic conditions. Six-day batch experiments were performed with soils constrained to different microbiological states, either by sterilisation or by adding organic substrates. Selenium was added to the soil as selenite. The distribution of selenium in the gaseous, liquid and solid phases of the batch was measured. Selenium partitioning between the various solid phases was investigated by chemical sequential extractions. Active microorganisms played major effects on the distribution of selenium within the soil. On the one hand, microorganisms could promote selenium volatilisation (in relatively small amounts), leading to the spreading of selenium compounds outside the soil. On the other hand, microbial activities increased both amount of selenium retained by the soil and the strength of its retention (less exchangeable selenium), making selenium less susceptible to remobilisation.
    Mots-clés : Biodegradation, Environmental, Selenium, Soil Microbiology, Soil Pollutants, Volatilization.

  • Haichar FZ, et al. 2008. Plant host habitat and root exudates shape soil bacterial community structure. The ISME journal. 2:1221-1230. doi: 10.1038/ismej.2008.80.
    Résumé : The rhizosphere is active and dynamic in which newly generated carbon, derived from root exudates, and ancient carbon, in soil organic matter (SOM), are available for microbial growth. Stable isotope probing (SIP) was used to determine bacterial communities assimilating each carbon source in the rhizosphere of four plant species. Wheat, maize, rape and barrel clover (Medicago truncatula) were grown separately in the same soil under (13)CO(2) (99% of atom (13)C) and DNA extracted from rhizosphere soil was fractionated by isopycnic centrifugation. Bacteria-assimilating root exudates were characterized by denaturing gradient gel electrophoresis (DGGE) analysis of (13)C-DNA and root DNA, whereas those assimilating SOM were identified from (12)C-DNA. Plant species root exudates significantly shaped rhizosphere bacterial community structure. Bacteria related to Sphingobacteriales and Myxococcus assimilated root exudates in colonizing roots of all four plants, whwereas bacteria related to Sphingomonadales utilized both carbon sources, and were identified in light, heavy and root compartment DNA. Sphingomonadales were specific to monocotyledons, whereas bacteria related to Enterobacter and Rhizobiales colonized all compartments of all four plants, used both fresh and ancient carbon and were considered as generalists. There was also evidence for an indirect important impact of root exudates, through stimulation of SOM assimilation by a diverse bacterial community.
    Mots-clés : Bacteria, Carbon Isotopes, Ecosystem, Molecular Sequence Data, Phylogeny, Plant Exudates, Plant Roots, Soil Microbiology.


  • Bernard L, et al. 2007. Dynamics and identification of soil microbial populations actively assimilating carbon from 13C-labelled wheat residue as estimated by DNA- and RNA-SIP techniques. Environmental microbiology. 9:752-764. doi: 10.1111/j.1462-2920.2006.01197.x.
    Résumé : This work is the first report on the use of DNA-, RNA-SIP approaches to elucidate the dynamics and the diversity of bacterial populations actively assimilating C derived from plant residues labelled at more than 90% (13)C. Wheat-residues, were incorporated and incubated into soil microcosms for 28 days. At the end of the incubation time, no more than 55% of the total CO(2) released was (13)C-labelled, suggesting the occurrence of an important priming effect process. After 7 days, more than 30% of the whole DNA extracted were labelled, allowing an efficient separation of labelled from unlabelled DNA using density gradient centrifugation. The genetic structure of bacterial community, assessed by Automated Ribosomal Intergenic Spacer Analysis technique, was deduced from the (13)C- and (12)C-fractions of control and enriched conditions, over the time course of the experiment. Dynamics showed that wheat residues directly induced a rapid and durable stimulation of fresh organic matter (FOM) degrading populations ((13)C), while specific soil organic matter (SOM) degrading populations ((12)C) seemed to be indirectly stimulated only at the early time point (t7d). After 14 days of incubations, 16S rRNA clone libraries were elaborated on (12)C- and (13)C-RNA extracted from enriched microcosms, as well as (12)C-RNA extracted from control condition. Stimulation of the beta- and gamma-subgroups of proteobacteria, where numerous populations were previously described as r-strategists or copiotrophic organisms, was recorded in the (13)C-fraction. In the mean time, several phyla like Actinobacteria, Cyanobacteria, Candidate, Gemmatimonadetes and Planctomycetes were only present in (12)C fractions. Surprisingly, several sequences affiliated to species characterized as oligotrophic organisms were retrieved in both types of fraction. Trophic relationships between soil bacteria involved in FOM and SOM degradation were discussed on the basis of different hypotheses of Fontaine and colleagues (2003) concerning the mechanisms of the priming effect induction.
    Mots-clés : Bacteria, Biodegradation, Environmental, Carbon Isotopes, Carbon Radioisotopes, DNA, Bacterial, Ecosystem, RNA, Bacterial, RNA, Ribosomal, 16S, Sequence Analysis, DNA, Soil Microbiology, Triticum.

  • Haichar FZ, et al. 2007. Identification of cellulolytic bacteria in soil by stable isotope probing. Environmental microbiology. 9:625-634. doi: 10.1111/j.1462-2920.2006.01182.x.
    Résumé : Plant residues, mainly made up of cellulose, are the largest fraction of organic carbon material in terrestrial ecosystems. Soil microorganisms are mainly responsible for the transfer of this carbon to the atmosphere, but their contribution is not accurately known. The aim of the present study was to identify bacterial populations that are actively involved in cellulose degradation, using the DNA-stable isotope probing (DNA-SIP) technique. (13)C-cellulose was produced by Acetobacter xylinus and incubated in soil for 7, 14, 30 and 90 days. Total DNA was extracted from the soil, the (13)C-labelled (heavy) and unlabelled (light) DNA fractions were separated by ultracentrifugation, and the structure of active bacterial communities was analysed by bacterial-automated ribosomal intergenic spacer analysis (B-ARISA) and characterized with denaturing gradient gel electrophoresis (DGGE). Cellulose degradation was associated with significant changes in bacterial community structure issued from heavy DNA, leading to the appearance of new bands and increase in relative intensities of other bands until day 30. The majority of bands decreased in relative intensity at day 90. Sequencing and phylogenetic analysis of 10 of these bands in DGGE profiles indicated that most sequences were closely related to sequences from organisms known for their ability to degrade cellulose or to uncultured soil bacteria.
    Mots-clés : Bacteria, Carbon Isotopes, Cellulose, Centrifugation, Density Gradient, DNA, Bacterial, DNA, Ribosomal Spacer, Ecosystem, Electrophoresis, Polyacrylamide Gel, Molecular Sequence Data, Phylogeny, RNA, Ribosomal, 16S, Sequence Analysis, DNA, Soil Microbiology.

Chapitre d’ouvrages


  • Achouak W, Haichar FZ. 2013. Shaping of microbial community structure and function in the rhizosphere by four diverse plant species. In: Molecular Microbial Ecology of the Rhizosphere. Frans J. de Bruijn, published by Wiley/Blackwell, ISBN p. .
    Mots-clés : #5.


  • Haichar FZ, Achouak W. 2010. Application of stable isotope probing (DNA-SIP) in the identification of cellulolytic soil bacteria and fungi. In: Cellulose Structure and Proprieties, Derivatives and Industrial Uses. Arnaud Lejeune & Thibaut Deprez, Nova Science Publishers, Inc, New York, p. .
    Mots-clés : #5.


  • Berge O, Balesdent J, Haichar FZ, Marol C, Achouak W. 2006. Root exudate-consuming microbial community structure by DNA stable isotope probing. In: Handbook of methods used in rhizosphere research. p. .

Article de journaux



  • Balesdent J, Haichar FZ, Berge O. 2006. Couplages isotopes stables outils moléculaires en écologie microbienne. Biofutur.
    Mots-clés : #5.



  • Bardon C, Poly F, Piola F, Haichar FZ, Comte G. 2015. Utilisation de proanthocyanidines pour lutter contre la dénitrification.
    Mots-clés : #3, #5, #cesn.

Communications Orales



  • Lecomte S, et al. 2016. Denitrification And Its Regulation In Agrobacterium fabrum C58.
    Mots-clés : #AME, #poster.