Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time

Plant specialized metabolites play an important role in soil carbon (C) and nutrient fluxes. Through anti-microbial effects, they can modulate microbial assemblages and associated microbial-driven processes, such as nutrient cycling, so to positively or negatively cascade on plant fitness. As such,...

Full description

Bibliographic Details
Main Authors: Samuel Hamard, Bjorn J. M. Robroek, Pierre-Marie Allard, Constant Signarbieux, Shuaizhen Zhou, Tongchai Saesong, Flore de Baaker, Alexandre Buttler, Geneviève Chiapusio, Jean-Luc Wolfender, Luca Bragazza, Vincent E. J. Jassey
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02042/full
id doaj-28fb2cdd2d864f75959f929f8fb97ff6
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Samuel Hamard
Samuel Hamard
Samuel Hamard
Samuel Hamard
Bjorn J. M. Robroek
Bjorn J. M. Robroek
Bjorn J. M. Robroek
Pierre-Marie Allard
Constant Signarbieux
Constant Signarbieux
Shuaizhen Zhou
Tongchai Saesong
Tongchai Saesong
Flore de Baaker
Alexandre Buttler
Alexandre Buttler
Alexandre Buttler
Geneviève Chiapusio
Geneviève Chiapusio
Jean-Luc Wolfender
Luca Bragazza
Luca Bragazza
Luca Bragazza
Vincent E. J. Jassey
Vincent E. J. Jassey
Vincent E. J. Jassey
spellingShingle Samuel Hamard
Samuel Hamard
Samuel Hamard
Samuel Hamard
Bjorn J. M. Robroek
Bjorn J. M. Robroek
Bjorn J. M. Robroek
Pierre-Marie Allard
Constant Signarbieux
Constant Signarbieux
Shuaizhen Zhou
Tongchai Saesong
Tongchai Saesong
Flore de Baaker
Alexandre Buttler
Alexandre Buttler
Alexandre Buttler
Geneviève Chiapusio
Geneviève Chiapusio
Jean-Luc Wolfender
Luca Bragazza
Luca Bragazza
Luca Bragazza
Vincent E. J. Jassey
Vincent E. J. Jassey
Vincent E. J. Jassey
Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
Frontiers in Microbiology
allelopathy and allelochemicals
metabolomics
microbial networks
microbial respiration and biomass
peatland
plant competition
author_facet Samuel Hamard
Samuel Hamard
Samuel Hamard
Samuel Hamard
Bjorn J. M. Robroek
Bjorn J. M. Robroek
Bjorn J. M. Robroek
Pierre-Marie Allard
Constant Signarbieux
Constant Signarbieux
Shuaizhen Zhou
Tongchai Saesong
Tongchai Saesong
Flore de Baaker
Alexandre Buttler
Alexandre Buttler
Alexandre Buttler
Geneviève Chiapusio
Geneviève Chiapusio
Jean-Luc Wolfender
Luca Bragazza
Luca Bragazza
Luca Bragazza
Vincent E. J. Jassey
Vincent E. J. Jassey
Vincent E. J. Jassey
author_sort Samuel Hamard
title Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
title_short Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
title_full Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
title_fullStr Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
title_full_unstemmed Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
title_sort effects of sphagnum leachate on competitive sphagnum microbiome depend on species and time
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-09-01
description Plant specialized metabolites play an important role in soil carbon (C) and nutrient fluxes. Through anti-microbial effects, they can modulate microbial assemblages and associated microbial-driven processes, such as nutrient cycling, so to positively or negatively cascade on plant fitness. As such, plant specialized metabolites can be used as a tool to supplant competitors. These compounds are little studied in bryophytes. This is especially notable in peatlands where Sphagnum mosses can dominate the vegetation and show strong interspecific competition. Sphagnum mosses form carpets where diverse microbial communities live and play a crucial role in Sphagnum fitness by regulating C and nutrient cycling. Here, by means of a microcosm experiment, we assessed to what extent moss metabolites of two Sphagnum species (S. fallax and S. divinum) modulate the competitive Sphagnum microbiome, with particular focus on microbial respiration. Using a reciprocal leachate experiment, we found that interactions between Sphagnum leachates and microbiome are species-specific. We show that both Sphagnum leachates differed in compound richness and compound relative abundance, especially sphagnum acid derivates, and that they include microbial-related metabolites. The addition of S. divinum leachate on the S. fallax microbiome immediately reduced microbial respiration (−95%). Prolonged exposition of S. fallax microbiome to S. divinum leachate destabilized the food web structure due to a modulation of microbial abundance. In particular, leachate addition decreased the biomass of testate amoebae and rotifers but increased that of ciliates. These changes did not influence microbial CO2 respiration, suggesting that the structural plasticity of the food web leads to its functional resistance through the replacement of species that are functionally redundant. In contrast, S. fallax leachate neither affected S. divinum microbial respiration, nor microbial biomass. We, however, found that S. fallax leachate addition stabilized the food web structure associated to S. divinum by changing trophic interactions among species. The differences in allelopathic effects between both Sphagnum leachates might impact their competitiveness and affect species distribution at local scale. Our study further paves the way to better understand the role of moss and microbial specialized metabolites in peatland C dynamics.
topic allelopathy and allelochemicals
metabolomics
microbial networks
microbial respiration and biomass
peatland
plant competition
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02042/full
work_keys_str_mv AT samuelhamard effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT samuelhamard effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT samuelhamard effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT samuelhamard effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT bjornjmrobroek effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT bjornjmrobroek effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT bjornjmrobroek effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT pierremarieallard effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT constantsignarbieux effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT constantsignarbieux effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT shuaizhenzhou effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT tongchaisaesong effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT tongchaisaesong effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT floredebaaker effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT alexandrebuttler effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT alexandrebuttler effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT alexandrebuttler effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT genevievechiapusio effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT genevievechiapusio effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT jeanlucwolfender effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT lucabragazza effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT lucabragazza effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT lucabragazza effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT vincentejjassey effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT vincentejjassey effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
AT vincentejjassey effectsofsphagnumleachateoncompetitivesphagnummicrobiomedependonspeciesandtime
_version_ 1724810094957297664
spelling doaj-28fb2cdd2d864f75959f929f8fb97ff62020-11-25T02:34:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-09-011010.3389/fmicb.2019.02042422446Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and TimeSamuel Hamard0Samuel Hamard1Samuel Hamard2Samuel Hamard3Bjorn J. M. Robroek4Bjorn J. M. Robroek5Bjorn J. M. Robroek6Pierre-Marie Allard7Constant Signarbieux8Constant Signarbieux9Shuaizhen Zhou10Tongchai Saesong11Tongchai Saesong12Flore de Baaker13Alexandre Buttler14Alexandre Buttler15Alexandre Buttler16Geneviève Chiapusio17Geneviève Chiapusio18Jean-Luc Wolfender19Luca Bragazza20Luca Bragazza21Luca Bragazza22Vincent E. J. Jassey23Vincent E. J. Jassey24Vincent E. J. Jassey25ECOLAB, Laboratoire d’Ecologie Fonctionnelle et Environnement, Université de Toulouse, CNRS, Toulouse, FranceLaboratory of Ecological Systems (ECOS), Ecole Polytechnique Fédérale de Lausanne (EPFL), School of Architecture, Civil and Environmental Engineering, Lausanne, SwitzerlandSwiss Federal Institute for Forest, Snow and Landscape Research (WSL), Lausanne, SwitzerlandLaboratoire de Géologie, UMR 8538, CNRS-ENS, Ecole Normale Supérieure, Paris, FranceLaboratory of Ecological Systems (ECOS), Ecole Polytechnique Fédérale de Lausanne (EPFL), School of Architecture, Civil and Environmental Engineering, Lausanne, SwitzerlandSchool of Biological Sciences, University of Southampton, Southampton, United KingdomAquatic Ecology and Environmental Biology Group, Faculty of Science, Institute for Water and Wetland Research, Radboud University, Nijmegen, NetherlandsSchool of Pharmaceutical Sciences, University of Geneva, University of Lausanne, Geneva, SwitzerlandLaboratory of Ecological Systems (ECOS), Ecole Polytechnique Fédérale de Lausanne (EPFL), School of Architecture, Civil and Environmental Engineering, Lausanne, SwitzerlandSwiss Federal Institute for Forest, Snow and Landscape Research (WSL), Lausanne, SwitzerlandSchool of Pharmaceutical Sciences, University of Geneva, University of Lausanne, Geneva, SwitzerlandSchool of Pharmaceutical Sciences, University of Geneva, University of Lausanne, Geneva, SwitzerlandDepartment of Pharmaceutical Chemistry and Pharmacognosy, Faculty of Pharmaceutical Sciences and Center of Excellence for Innovation in Chemistry, Naresuan University, Phitsanulok, ThailandSchool of Pharmaceutical Sciences, University of Geneva, University of Lausanne, Geneva, SwitzerlandLaboratory of Ecological Systems (ECOS), Ecole Polytechnique Fédérale de Lausanne (EPFL), School of Architecture, Civil and Environmental Engineering, Lausanne, SwitzerlandSwiss Federal Institute for Forest, Snow and Landscape Research (WSL), Lausanne, SwitzerlandLaboratoire Chrono-Environnement, Université Bourgogne Franche Comté, UMR CNRS 6249 USC INRA, Montbéliard, FranceLaboratoire Chrono-Environnement, Université Bourgogne Franche Comté, UMR CNRS 6249 USC INRA, Montbéliard, France0Laboratoire Carrtel, Université Savoie Mont Blanc INRA 042, Domaine Universitaire Belledonne, Le Bourget-du-Lac, FranceSchool of Pharmaceutical Sciences, University of Geneva, University of Lausanne, Geneva, SwitzerlandLaboratory of Ecological Systems (ECOS), Ecole Polytechnique Fédérale de Lausanne (EPFL), School of Architecture, Civil and Environmental Engineering, Lausanne, SwitzerlandSwiss Federal Institute for Forest, Snow and Landscape Research (WSL), Lausanne, Switzerland1Department of Life Science and Biotechnologies, University of Ferrara, Ferrara, ItalyECOLAB, Laboratoire d’Ecologie Fonctionnelle et Environnement, Université de Toulouse, CNRS, Toulouse, FranceLaboratory of Ecological Systems (ECOS), Ecole Polytechnique Fédérale de Lausanne (EPFL), School of Architecture, Civil and Environmental Engineering, Lausanne, SwitzerlandSwiss Federal Institute for Forest, Snow and Landscape Research (WSL), Lausanne, SwitzerlandPlant specialized metabolites play an important role in soil carbon (C) and nutrient fluxes. Through anti-microbial effects, they can modulate microbial assemblages and associated microbial-driven processes, such as nutrient cycling, so to positively or negatively cascade on plant fitness. As such, plant specialized metabolites can be used as a tool to supplant competitors. These compounds are little studied in bryophytes. This is especially notable in peatlands where Sphagnum mosses can dominate the vegetation and show strong interspecific competition. Sphagnum mosses form carpets where diverse microbial communities live and play a crucial role in Sphagnum fitness by regulating C and nutrient cycling. Here, by means of a microcosm experiment, we assessed to what extent moss metabolites of two Sphagnum species (S. fallax and S. divinum) modulate the competitive Sphagnum microbiome, with particular focus on microbial respiration. Using a reciprocal leachate experiment, we found that interactions between Sphagnum leachates and microbiome are species-specific. We show that both Sphagnum leachates differed in compound richness and compound relative abundance, especially sphagnum acid derivates, and that they include microbial-related metabolites. The addition of S. divinum leachate on the S. fallax microbiome immediately reduced microbial respiration (−95%). Prolonged exposition of S. fallax microbiome to S. divinum leachate destabilized the food web structure due to a modulation of microbial abundance. In particular, leachate addition decreased the biomass of testate amoebae and rotifers but increased that of ciliates. These changes did not influence microbial CO2 respiration, suggesting that the structural plasticity of the food web leads to its functional resistance through the replacement of species that are functionally redundant. In contrast, S. fallax leachate neither affected S. divinum microbial respiration, nor microbial biomass. We, however, found that S. fallax leachate addition stabilized the food web structure associated to S. divinum by changing trophic interactions among species. The differences in allelopathic effects between both Sphagnum leachates might impact their competitiveness and affect species distribution at local scale. Our study further paves the way to better understand the role of moss and microbial specialized metabolites in peatland C dynamics.https://www.frontiersin.org/article/10.3389/fmicb.2019.02042/fullallelopathy and allelochemicalsmetabolomicsmicrobial networksmicrobial respiration and biomasspeatlandplant competition