Cargando…

Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest

Drought impacts on microbial activity can alter soil carbon fate and lead to the loss of stored carbon to the atmosphere as CO(2) and volatile organic compounds (VOCs). Here we examined drought impacts on carbon allocation by soil microbes in the Biosphere 2 artificial tropical rainforest by trackin...

Descripción completa

Detalles Bibliográficos
Autores principales: Honeker, Linnea K., Pugliese, Giovanni, Ingrisch, Johannes, Fudyma, Jane, Gil-Loaiza, Juliana, Carpenter, Elizabeth, Singer, Esther, Hildebrand, Gina, Shi, Lingling, Hoyt, David W., Chu, Rosalie K., Toyoda, Jason, Krechmer, Jordan E., Claflin, Megan S., Ayala-Ortiz, Christian, Freire-Zapata, Viviana, Pfannerstill, Eva Y., Daber, L. Erik, Meeran, Kathiravan, Dippold, Michaela A., Kreuzwieser, Jürgen, Williams, Jonathan, Ladd, S. Nemiah, Werner, Christiane, Tfaily, Malak M., Meredith, Laura K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10390333/
https://www.ncbi.nlm.nih.gov/pubmed/37524975
http://dx.doi.org/10.1038/s41564-023-01432-9
_version_ 1785082456161910784
author Honeker, Linnea K.
Pugliese, Giovanni
Ingrisch, Johannes
Fudyma, Jane
Gil-Loaiza, Juliana
Carpenter, Elizabeth
Singer, Esther
Hildebrand, Gina
Shi, Lingling
Hoyt, David W.
Chu, Rosalie K.
Toyoda, Jason
Krechmer, Jordan E.
Claflin, Megan S.
Ayala-Ortiz, Christian
Freire-Zapata, Viviana
Pfannerstill, Eva Y.
Daber, L. Erik
Meeran, Kathiravan
Dippold, Michaela A.
Kreuzwieser, Jürgen
Williams, Jonathan
Ladd, S. Nemiah
Werner, Christiane
Tfaily, Malak M.
Meredith, Laura K.
author_facet Honeker, Linnea K.
Pugliese, Giovanni
Ingrisch, Johannes
Fudyma, Jane
Gil-Loaiza, Juliana
Carpenter, Elizabeth
Singer, Esther
Hildebrand, Gina
Shi, Lingling
Hoyt, David W.
Chu, Rosalie K.
Toyoda, Jason
Krechmer, Jordan E.
Claflin, Megan S.
Ayala-Ortiz, Christian
Freire-Zapata, Viviana
Pfannerstill, Eva Y.
Daber, L. Erik
Meeran, Kathiravan
Dippold, Michaela A.
Kreuzwieser, Jürgen
Williams, Jonathan
Ladd, S. Nemiah
Werner, Christiane
Tfaily, Malak M.
Meredith, Laura K.
author_sort Honeker, Linnea K.
collection PubMed
description Drought impacts on microbial activity can alter soil carbon fate and lead to the loss of stored carbon to the atmosphere as CO(2) and volatile organic compounds (VOCs). Here we examined drought impacts on carbon allocation by soil microbes in the Biosphere 2 artificial tropical rainforest by tracking (13)C from position-specific (13)C-pyruvate into CO(2) and VOCs in parallel with multi-omics. During drought, efflux of (13)C-enriched acetate, acetone and C(4)H(6)O(2) (diacetyl) increased. These changes represent increased production and buildup of intermediate metabolites driven by decreased carbon cycling efficiency. Simultaneously,(13)C-CO(2) efflux decreased, driven by a decrease in microbial activity. However, the microbial carbon allocation to energy gain relative to biosynthesis was unchanged, signifying maintained energy demand for biosynthesis of VOCs and other drought-stress-induced pathways. Overall, while carbon loss to the atmosphere via CO(2) decreased during drought, carbon loss via efflux of VOCs increased, indicating microbially induced shifts in soil carbon fate.
format Online
Article
Text
id pubmed-10390333
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-103903332023-08-02 Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest Honeker, Linnea K. Pugliese, Giovanni Ingrisch, Johannes Fudyma, Jane Gil-Loaiza, Juliana Carpenter, Elizabeth Singer, Esther Hildebrand, Gina Shi, Lingling Hoyt, David W. Chu, Rosalie K. Toyoda, Jason Krechmer, Jordan E. Claflin, Megan S. Ayala-Ortiz, Christian Freire-Zapata, Viviana Pfannerstill, Eva Y. Daber, L. Erik Meeran, Kathiravan Dippold, Michaela A. Kreuzwieser, Jürgen Williams, Jonathan Ladd, S. Nemiah Werner, Christiane Tfaily, Malak M. Meredith, Laura K. Nat Microbiol Article Drought impacts on microbial activity can alter soil carbon fate and lead to the loss of stored carbon to the atmosphere as CO(2) and volatile organic compounds (VOCs). Here we examined drought impacts on carbon allocation by soil microbes in the Biosphere 2 artificial tropical rainforest by tracking (13)C from position-specific (13)C-pyruvate into CO(2) and VOCs in parallel with multi-omics. During drought, efflux of (13)C-enriched acetate, acetone and C(4)H(6)O(2) (diacetyl) increased. These changes represent increased production and buildup of intermediate metabolites driven by decreased carbon cycling efficiency. Simultaneously,(13)C-CO(2) efflux decreased, driven by a decrease in microbial activity. However, the microbial carbon allocation to energy gain relative to biosynthesis was unchanged, signifying maintained energy demand for biosynthesis of VOCs and other drought-stress-induced pathways. Overall, while carbon loss to the atmosphere via CO(2) decreased during drought, carbon loss via efflux of VOCs increased, indicating microbially induced shifts in soil carbon fate. Nature Publishing Group UK 2023-07-31 2023 /pmc/articles/PMC10390333/ /pubmed/37524975 http://dx.doi.org/10.1038/s41564-023-01432-9 Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Honeker, Linnea K.
Pugliese, Giovanni
Ingrisch, Johannes
Fudyma, Jane
Gil-Loaiza, Juliana
Carpenter, Elizabeth
Singer, Esther
Hildebrand, Gina
Shi, Lingling
Hoyt, David W.
Chu, Rosalie K.
Toyoda, Jason
Krechmer, Jordan E.
Claflin, Megan S.
Ayala-Ortiz, Christian
Freire-Zapata, Viviana
Pfannerstill, Eva Y.
Daber, L. Erik
Meeran, Kathiravan
Dippold, Michaela A.
Kreuzwieser, Jürgen
Williams, Jonathan
Ladd, S. Nemiah
Werner, Christiane
Tfaily, Malak M.
Meredith, Laura K.
Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
title Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
title_full Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
title_fullStr Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
title_full_unstemmed Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
title_short Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
title_sort drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10390333/
https://www.ncbi.nlm.nih.gov/pubmed/37524975
http://dx.doi.org/10.1038/s41564-023-01432-9
work_keys_str_mv AT honekerlinneak droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT pugliesegiovanni droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT ingrischjohannes droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT fudymajane droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT gilloaizajuliana droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT carpenterelizabeth droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT singeresther droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT hildebrandgina droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT shilingling droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT hoytdavidw droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT churosaliek droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT toyodajason droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT krechmerjordane droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT claflinmegans droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT ayalaortizchristian droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT freirezapataviviana droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT pfannerstillevay droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT daberlerik droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT meerankathiravan droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT dippoldmichaelaa droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT kreuzwieserjurgen droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT williamsjonathan droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT laddsnemiah droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT wernerchristiane droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT tfailymalakm droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest
AT meredithlaurak droughtreroutessoilmicrobialcarbonmetabolismtowardsemissionofvolatilemetabolitesinanartificialtropicalrainforest