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1. Plant host habitat and root exudates shape fungal diversity

Author

Mylène Hugoni, Julien P. Guyonnet, Patricia Luis, Feth el Zahar Haichar, 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-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), and CNRS EC2CO research programs

Subjects
0106 biological sciences, 0301 basic medicine, Exudate, Mycobiota, [SDV]Life Sciences [q-bio], Plant Science, Plant nutrient-use strategies, Biology, Poaceae, Root exudates, DNA, Ribosomal, Plant Roots, 01 natural sciences, Glomeromycota, 03 medical and health sciences, Mycorrhizae, Botany, RNA, Ribosomal, 18S, Genetics, medicine, DNA, Fungal, Molecular Biology, Phylogeny, Soil Microbiology, Ecology, Evolution, Behavior and Systematics, Glomus, 2. Zero hunger, Rhizosphere, Active fungal communities, Microbiota, Soil organic matter, fungi, food and beverages, Species diversity, Sequence Analysis, DNA, General Medicine, 15. Life on land, biology.organism_classification, 030104 developmental biology, Isotope Labeling, Stable-isotope probing, DNA, Intergenic, medicine.symptom, Soil microbiology, 010606 plant biology & botany
Abstract

The rhizospheric microbiome is clearly affected by plant species and certain of their functional traits. These functional traits allow plants to adapt to their environmental conditions by acquiring or conserving nutrients, thus defining different ecological resource-use plant strategies. In the present study, we investigated whether plants with one of the two nutrient-use strategies (conservative versus exploitative) could influence fungal communities involved in soil organic matter degradation and root exudate assimilation, as well as those colonizing root tissues. We applied a DNA-based, stable-isotope probing (DNA-SIP) approach to four grass species distributed along a gradient of plant nutrient resource strategies, ranging from conservative to exploitative species, and analyzed their associated mycobiota composition using a fungal internal transcribed spacer (ITS) and Glomeromycotina 18S rRNA gene metabarcoding approach. Our results demonstrated that fungal taxa associated with exploitative and conservative plants could be separated into two general categories according to their location: generalists, which are broadly distributed among plants from each strategy and represent the core mycobiota of soil organic matter degraders, root exudate consumers in the root-adhering soil, and root colonizers; and specialists, which are locally abundant in one species and more specifically involved in soil organic matter degradation or root exudate assimilation on the root-adhering soil and the root tissues. Interestingly, for arbuscular mycorrhizal fungi analysis, all plant roots were mainly colonized by Glomus species, whereas an increased diversity of Glomeromycotina genera was observed for the exploitative plant species Dactylis glomerata.

Published
2018
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2. Plant Nutrient Resource Use Strategies Shape Active Rhizosphere Microbiota Through Root Exudation

Author

Julien P, Guyonnet, Martin, Guillemet, Audrey, Dubost, Laurent, Simon, Philippe, Ortet, Mohamed, Barakat, Thierry, Heulin, Wafa, Achouak, Feth El Zahar, Haichar, 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), Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés (LEHNA), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS), Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB) (BIAM), 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)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Ecosystèmes continentaux et risques environnementaux (ECCOREV), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Laboratoire d'Ecologie Microbienne de la Rhizosphère et d'Environnements Extrêmes (LEMIRE), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), EC2CO-MicrobiEn (CNRS), 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)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-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), and 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)

Subjects
denitrification, microbial activities, plant nutrient use strategies, [SDV]Life Sciences [q-bio], microbiota, active bacterial community, stable isotope probing (SIP), Plant Science, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, rhizosphere, root exudation, ComputingMilieux_MISCELLANEOUS, Original Research
Abstract

International audience; Plant strategies for soil nutrient uptake have the potential to strongly influence plant-microbiota interactions, due to the competition between plants and microorganisms for soil nutrient acquisition and/or conservation. In the present study, we investigate whether these plant strategies could influence rhizosphere microbial activities via root exudation, and contribute to the microbiota diversification of active bacterial communities colonizing the root-adhering soil (RAS) and inhabiting the root tissues. We applied a DNA-based stable isotope probing (DNA-SIP) approach to six grass species distributed along a gradient of plant nutrient resource strategies, from conservative species, characterized by low nitrogen (N) uptake, a long lifespans and low root exudation level, to exploitative species, characterized by high rates of photosynthesis, rapid rates of N uptake and high root exudation level. We analyzed their (i) associated microbiota composition involved in root exudate assimilation and soil organic matter (SOM) degradation by 16S-rRNA-based metabarcoding. (ii) We determine the impact of root exudation level on microbial activities (denitrification and respiration) by gas chromatography. Measurement of microbial activities revealed an increase in denitrification and respiration activities for microbial communities colonizing the RAS of exploitative species. This increase of microbial activities results probably from a higher exudation rate and more diverse metabolites by exploitative plant species. Furthermore, our results demonstrate that plant nutrient resource strategies have a role in shaping active microbiota. We present evidence demonstrating that plant nutrient use strategies shape active microbiota involved in root exudate assimilation and SOM degradation via root exudation.

Published
2018
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3. The effects of plant nutritional strategy on soil microbial denitrification activity through rhizosphere primary metabolites

Author

Amélie A. M. Cantarel, Julien P. Guyonnet, Guillaume Meiffren, Serge Michalet, Gilles Comte, Feth el Zahar Haichar, Clément Labois, Florian Vautrin, 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-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), 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
0106 biological sciences, 0301 basic medicine, Denitrification, enzymic activity, dénitrification, sol, [SDV]Life Sciences [q-bio], root extract, Poaceae, 01 natural sciences, Applied Microbiology and Biotechnology, Microbiology, Plant Roots, soil, 03 medical and health sciences, Nutrient, denitrification enzyme activity without carbon addition, Botany, élément nutritif, Plant Physiological Phenomena, Soil Microbiology, Bromus erectus, 2. Zero hunger, Rhizosphere, Ecology, biology, [ SDV ] Life Sciences [q-bio], Nutrient management, activité enzymatique, Primary metabolite, 15. Life on land, biology.organism_classification, root, Carbon, racine, 030104 developmental biology, Microbial population biology, Agronomy, plant nutrient management strategies, Soil water, plante, root adhering-soil, primary metabolites, rhizosphère, métabolite primaire, 010606 plant biology & botany
Abstract

The aim of this study was to determine (i) whether plant nutritional strategy affects the composition of primary metabolites exuded into the rhizosphere and (ii) the impact of exuded metabolites on denitrification activity in soil. We answered this question by analysing primary metabolite content extracted from the root-adhering soil (RAS) and the roots of three grasses representing different nutrient management strategies: conservative (Festuca paniculata), intermediate (Bromus erectus) and exploitative (Dactylis glomerata). We also investigated the impact of primary metabolites on soil microbial denitrification enzyme activity without carbon addition, comparing for each plant RAS and bulk soils. Our data show that plant nutritional strategy impacts on primary metabolite composition of root extracts or RAS. Further we show, for the first time, that RAS-extracted primary metabolites are probably better indicators to explain plant nutrient strategy than root-extracted ones. In addition, our results show that some primary metabolites present in the RAS were well correlated with soil microbial denitrification activity with positive relationships found between denitrification and the presence of some organic acids and negative ones with the presence of xylose. We demonstrated that the analysis of primary metabolites extracted from the RAS is probably more pertinent to evaluate the impact of plant on soil microbial community functioning.

Published
2017
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4. Titanium dioxide nanoparticles strongly impact soil microbial function by affecting archaeal nitrifiers

Author

Thomas Pommier, Agnès Richaume, Marie Simonin, Julien P. Guyonnet, Audrey Dubost, Jean M.F. Martins, 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 ), Université Claude Bernard Lyon 1 ( UCBL ), Université de Lyon, Centre National de la Recherche Scientifique ( CNRS ), Center for the Environmental Implications of Nanotechnology, Duke University, Department of Biology, Northern Arizona University [Flagstaff], UMR 5564 Laboratoire d'étude des Transferts en Hydrologie et Environnement (LTHE), Université Grenoble Alpes ( UGA ), Rhone-Alpes Region - ARC Environnement, French National Program EC2CO-CNRS AT-Microbien, 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), Université Claude Bernard Lyon 1 (UCBL), Centre National de la Recherche Scientifique (CNRS), Université Grenoble Alpes (UGA), 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), Observatoire des Sciences de l'Univers de Grenoble (OSUG ), Institut polytechnique de Grenoble - Grenoble Institute of Technology (Grenoble INP )-Institut national des sciences de l'Univers (INSU - CNRS)-Institut national de recherche en sciences et technologies pour l'environnement et l'agriculture (IRSTEA)-Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry])-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes [2016-2019] (UGA [2016-2019]), and Richaume-Jolion, Agnès

Subjects
2. Zero hunger, 0301 basic medicine, Soil health, Multidisciplinary, Denitrification, [ SDV ] Life Sciences [q-bio], Ecology, [SDV]Life Sciences [q-bio], Microorganism, technology, industry, and agriculture, 15. Life on land, 010501 environmental sciences, 01 natural sciences, Article, 03 medical and health sciences, 030104 developmental biology, Microbial population biology, 13. Climate action, Soil water, Environmental science, Nitrification, Ecosystem, Nitrogen cycle, 0105 earth and related environmental sciences
Abstract

Soils are facing new environmental stressors, such as titanium dioxide nanoparticles (TiO2-NPs). While these emerging pollutants are increasingly released into most ecosystems, including agricultural fields, their potential impacts on soil and its function remain to be investigated. Here we report the response of the microbial community of an agricultural soil exposed over 90 days to TiO2-NPs (1 and 500 mg kg−1 dry soil). To assess their impact on soil function, we focused on the nitrogen cycle and measured nitrification and denitrification enzymatic activities and by quantifying specific representative genes (amoA for ammonia-oxidizers, nirK and nirS for denitrifiers). Additionally, diversity shifts were examined in bacteria, archaea, and the ammonia-oxidizing clades of each domain. With strong negative impacts on nitrification enzyme activities and the abundances of ammonia-oxidizing microorganism, TiO2-NPs triggered cascading negative effects on denitrification enzyme activity and a deep modification of the bacterial community structure after just 90 days of exposure to even the lowest, realistic concentration of NPs. These results appeal further research to assess how these emerging pollutants modify the soil health and broader ecosystem function.

Published
2016
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5. Stable isotope probing of carbon flow in the plant holobiont

Author

Thierry Heulin, Wafa Achouak, Julien P. Guyonnet, Feth el Zahar Haichar, 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-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), Centre National de la Recherche Scientifique (CNRS), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon, Biologie végétale et microbiologie environnementale - UMR7265 (BVME), Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB) (BIAM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-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)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-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), Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Ecosystèmes continentaux et risques environnementaux (ECCOREV), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), French National Research Agency (ANR CESA IMA-GMO), 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)-Aix Marseille Université (AMU)-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)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), 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), 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)-Aix Marseille Université (AMU)-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 ), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique ( INRA ) -VetAgro Sup ( VAS ), Centre National de la Recherche Scientifique ( CNRS ), Université Claude Bernard Lyon 1 ( UCBL ), Biologie végétale et microbiologie environnementale - UMR7265 ( BVME ), Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Aix Marseille Université ( AMU ), Commissariat à l'Energie Atomique et aux Energies Alternatives, Ecosystèmes continentaux et risques environnementaux ( ECCOREV ), and Aix Marseille Université ( AMU ) -Centre National de la Recherche Scientifique ( CNRS )

Subjects
0301 basic medicine, Rhizosphere, Carbon Isotopes, [ SDV ] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], Biomedical Engineering, Stable-isotope probing, food and beverages, Bioengineering, Biology, Plants, Plant Roots, Carbon cycle, Holobiont, 03 medical and health sciences, 030104 developmental biology, Isotopes of carbon, Isotope Labeling, Botany, Carbon flow, Soil microbiology, Plant genes, Soil Microbiology, Biotechnology
Abstract

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 C-13 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.

Published
2016
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