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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,...

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Autores principales: Hamard, Samuel, Robroek, Bjorn J. M., Allard, Pierre-Marie, Signarbieux, Constant, Zhou, Shuaizhen, Saesong, Tongchai, de Baaker, Flore, Buttler, Alexandre, Chiapusio, Geneviève, Wolfender, Jean-Luc, Bragazza, Luca, Jassey, Vincent E. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6742715/
https://www.ncbi.nlm.nih.gov/pubmed/31555245
http://dx.doi.org/10.3389/fmicb.2019.02042
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author Hamard, Samuel
Robroek, Bjorn J. M.
Allard, Pierre-Marie
Signarbieux, Constant
Zhou, Shuaizhen
Saesong, Tongchai
de Baaker, Flore
Buttler, Alexandre
Chiapusio, Geneviève
Wolfender, Jean-Luc
Bragazza, Luca
Jassey, Vincent E. J.
author_facet Hamard, Samuel
Robroek, Bjorn J. M.
Allard, Pierre-Marie
Signarbieux, Constant
Zhou, Shuaizhen
Saesong, Tongchai
de Baaker, Flore
Buttler, Alexandre
Chiapusio, Geneviève
Wolfender, Jean-Luc
Bragazza, Luca
Jassey, Vincent E. J.
author_sort Hamard, Samuel
collection PubMed
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 CO(2) 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.
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spelling pubmed-67427152019-09-25 Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time Hamard, Samuel Robroek, Bjorn J. M. Allard, Pierre-Marie Signarbieux, Constant Zhou, Shuaizhen Saesong, Tongchai de Baaker, Flore Buttler, Alexandre Chiapusio, Geneviève Wolfender, Jean-Luc Bragazza, Luca Jassey, Vincent E. J. Front Microbiol Microbiology 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 CO(2) 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. Frontiers Media S.A. 2019-09-06 /pmc/articles/PMC6742715/ /pubmed/31555245 http://dx.doi.org/10.3389/fmicb.2019.02042 Text en Copyright © 2019 Hamard, Robroek, Allard, Signarbieux, Zhou, Saesong, de Baaker, Buttler, Chiapusio, Wolfender, Bragazza and Jassey. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hamard, Samuel
Robroek, Bjorn J. M.
Allard, Pierre-Marie
Signarbieux, Constant
Zhou, Shuaizhen
Saesong, Tongchai
de Baaker, Flore
Buttler, Alexandre
Chiapusio, Geneviève
Wolfender, Jean-Luc
Bragazza, Luca
Jassey, Vincent E. J.
Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time
title 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_short 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
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6742715/
https://www.ncbi.nlm.nih.gov/pubmed/31555245
http://dx.doi.org/10.3389/fmicb.2019.02042
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