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Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities

Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well s...

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Autores principales: Chou, Ming-Yi, Andersen, Trine B., Mechan Llontop, Marco E., Beculheimer, Nick, Sow, Alassane, Moreno, Nick, Shade, Ashley, Hamberger, Bjoern, Bonito, Gregory
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580827/
https://www.ncbi.nlm.nih.gov/pubmed/37772854
http://dx.doi.org/10.1128/spectrum.01332-23
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author Chou, Ming-Yi
Andersen, Trine B.
Mechan Llontop, Marco E.
Beculheimer, Nick
Sow, Alassane
Moreno, Nick
Shade, Ashley
Hamberger, Bjoern
Bonito, Gregory
author_facet Chou, Ming-Yi
Andersen, Trine B.
Mechan Llontop, Marco E.
Beculheimer, Nick
Sow, Alassane
Moreno, Nick
Shade, Ashley
Hamberger, Bjoern
Bonito, Gregory
author_sort Chou, Ming-Yi
collection PubMed
description Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well studied, how different terpenes impact plant microbiomes belowground is much less understood. Here we designed an experiment to assess how belowground exogenous applications of monoterpenes (1,8-cineole and linalool) and a sesquiterpene (nerolidol) delivered through an artificial root system impacted its belowground bacterial and fungal microbiome. We found that the terpene applications had significant and variable impacts on bacterial and fungal communities, depending on terpene class and concentration; however, these impacts were localized to the artificial root system and the fungal rhizosphere. We complemented this experiment with pure culture bioassays on responsive bacteria and fungi isolated from the sorghum rhizobiome. Overall, higher concentrations (200 µM) of nerolidol were inhibitory to Ferrovibrium and tested Firmicutes. While fungal isolates of Penicillium and Periconia were also more inhibited by higher concentrations (200 µM) of nerolidol, Clonostachys was enhanced at this higher level and together with Humicola was inhibited by the lower concentration tested (100 µM). On the other hand, 1,8-cineole had an inhibitory effect on Orbilia at both tested concentrations but had a promotive effect at 100 µM on Penicillium and Periconia. Similarly, linalool at 100 µM had significant growth promotion in Mortierella, but an inhibitory effect for Orbilia. Together, these results highlight the variable direct effects of terpenes on single microbial isolates and demonstrate the complexity of microbe-terpene interactions in the rhizobiome. IMPORTANCE: Terpenes represent one of the largest and oldest classes of plant-specialized metabolism, but their role in the belowground microbiome is poorly understood. Here, we used a “rhizobox” mesocosm experimental set-up to supply different concentrations and classes of terpenes into the soil compartment with growing sorghum for 1 month to assess how these terpenes affect sorghum bacterial and fungal rhizobiome communities. Changes in bacterial and fungal communities between treatments belowground were characterized, followed by bioassays screening on bacterial and fungal isolates from the sorghum rhizosphere against terpenes to validate direct microbial responses. We found that microbial growth stimulatory and inhibitory effects were localized, terpene specific, dose dependent, and transient in time. This work paves the way for engineering terpene metabolisms in plant microbiomes for improved sustainable agriculture and bioenergy crop production.
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spelling pubmed-105808272023-10-18 Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities Chou, Ming-Yi Andersen, Trine B. Mechan Llontop, Marco E. Beculheimer, Nick Sow, Alassane Moreno, Nick Shade, Ashley Hamberger, Bjoern Bonito, Gregory Microbiol Spectr Research Article Terpenes are among the oldest and largest class of plant-specialized bioproducts that are known to affect plant development, adaptation, and biological interactions. While their biosynthesis, evolution, and function in aboveground interactions with insects and individual microbial species are well studied, how different terpenes impact plant microbiomes belowground is much less understood. Here we designed an experiment to assess how belowground exogenous applications of monoterpenes (1,8-cineole and linalool) and a sesquiterpene (nerolidol) delivered through an artificial root system impacted its belowground bacterial and fungal microbiome. We found that the terpene applications had significant and variable impacts on bacterial and fungal communities, depending on terpene class and concentration; however, these impacts were localized to the artificial root system and the fungal rhizosphere. We complemented this experiment with pure culture bioassays on responsive bacteria and fungi isolated from the sorghum rhizobiome. Overall, higher concentrations (200 µM) of nerolidol were inhibitory to Ferrovibrium and tested Firmicutes. While fungal isolates of Penicillium and Periconia were also more inhibited by higher concentrations (200 µM) of nerolidol, Clonostachys was enhanced at this higher level and together with Humicola was inhibited by the lower concentration tested (100 µM). On the other hand, 1,8-cineole had an inhibitory effect on Orbilia at both tested concentrations but had a promotive effect at 100 µM on Penicillium and Periconia. Similarly, linalool at 100 µM had significant growth promotion in Mortierella, but an inhibitory effect for Orbilia. Together, these results highlight the variable direct effects of terpenes on single microbial isolates and demonstrate the complexity of microbe-terpene interactions in the rhizobiome. IMPORTANCE: Terpenes represent one of the largest and oldest classes of plant-specialized metabolism, but their role in the belowground microbiome is poorly understood. Here, we used a “rhizobox” mesocosm experimental set-up to supply different concentrations and classes of terpenes into the soil compartment with growing sorghum for 1 month to assess how these terpenes affect sorghum bacterial and fungal rhizobiome communities. Changes in bacterial and fungal communities between treatments belowground were characterized, followed by bioassays screening on bacterial and fungal isolates from the sorghum rhizosphere against terpenes to validate direct microbial responses. We found that microbial growth stimulatory and inhibitory effects were localized, terpene specific, dose dependent, and transient in time. This work paves the way for engineering terpene metabolisms in plant microbiomes for improved sustainable agriculture and bioenergy crop production. American Society for Microbiology 2023-09-29 /pmc/articles/PMC10580827/ /pubmed/37772854 http://dx.doi.org/10.1128/spectrum.01332-23 Text en Copyright © 2023 Chou et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Chou, Ming-Yi
Andersen, Trine B.
Mechan Llontop, Marco E.
Beculheimer, Nick
Sow, Alassane
Moreno, Nick
Shade, Ashley
Hamberger, Bjoern
Bonito, Gregory
Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
title Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
title_full Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
title_fullStr Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
title_full_unstemmed Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
title_short Terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
title_sort terpenes modulate bacterial and fungal growth and sorghum rhizobiome communities
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10580827/
https://www.ncbi.nlm.nih.gov/pubmed/37772854
http://dx.doi.org/10.1128/spectrum.01332-23
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