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Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat

BACKGROUND: Understanding how elevated atmospheric CO(2) (eCO(2)) impacts on phosphorus (P) transformation in plant rhizosphere is critical for maintaining ecological sustainability in response to climate change, especially in agricultural systems where soil P availability is low. METHODS: This stud...

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Autores principales: Jin, Jian, Krohn, Christian, Franks, Ashley E., Wang, Xiaojuan, Wood, Jennifer L., Petrovski, Steve, McCaskill, Malcolm, Batinovic, Steven, Xie, Zhihuang, Tang, Caixian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8785599/
https://www.ncbi.nlm.nih.gov/pubmed/35074003
http://dx.doi.org/10.1186/s40168-021-01203-w
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author Jin, Jian
Krohn, Christian
Franks, Ashley E.
Wang, Xiaojuan
Wood, Jennifer L.
Petrovski, Steve
McCaskill, Malcolm
Batinovic, Steven
Xie, Zhihuang
Tang, Caixian
author_facet Jin, Jian
Krohn, Christian
Franks, Ashley E.
Wang, Xiaojuan
Wood, Jennifer L.
Petrovski, Steve
McCaskill, Malcolm
Batinovic, Steven
Xie, Zhihuang
Tang, Caixian
author_sort Jin, Jian
collection PubMed
description BACKGROUND: Understanding how elevated atmospheric CO(2) (eCO(2)) impacts on phosphorus (P) transformation in plant rhizosphere is critical for maintaining ecological sustainability in response to climate change, especially in agricultural systems where soil P availability is low. METHODS: This study used rhizoboxes to physically separate rhizosphere regions (plant root-soil interface) into 1.5-mm segments. Wheat plants were grown in rhizoboxes under eCO(2) (800 ppm) and ambient CO(2) (400 ppm) in two farming soils, Chromosol and Vertosol, supplemented with phytate (organic P). Photosynthetic carbon flow in the plant-soil continuum was traced with (13)CO(2) labeling. Amplicon sequencing was performed on the rhizosphere-associated microbial community in the root-growth zone, and 1.5 mm and 3 mm away from the root. RESULTS: Elevated CO(2) accelerated the mineralization of phytate in the rhizosphere zones, which corresponded with increases in plant-derived (13)C enrichment and the relative abundances of discreet phylogenetic clades containing Bacteroidetes and Gemmatimonadetes in the bacterial community, and Funneliformis affiliated to arbuscular mycorrhizas in the fungal community. Although the amplicon sequence variants (ASVs) associated the stimulation of phytate mineralization under eCO(2) differed between the two soils, these ASVs belonged to the same phyla associated with phytase and phosphatase production. The symbiotic mycorrhizas in the rhizosphere of wheat under eCO(2) benefited from increased plant C supply and increased P access from soil. Further supportive evidence was the eCO(2)-induced increase in the genetic pool expressing the pentose phosphate pathway, which is the central pathway for biosynthesis of RNA/DNA precursors. CONCLUSIONS: The results suggested that an increased belowground carbon flow under eCO(2) stimulated bacterial growth, changing community composition in favor of phylotypes capable of degrading aromatic P compounds. It is proposed that energy investments by bacteria into anabolic processes increase under eCO(2) to level microbial P-use efficiencies and that synergies with symbiotic mycorrhizas further enhance the competition for and mineralization of organic P. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01203-w.
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spelling pubmed-87855992022-01-24 Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat Jin, Jian Krohn, Christian Franks, Ashley E. Wang, Xiaojuan Wood, Jennifer L. Petrovski, Steve McCaskill, Malcolm Batinovic, Steven Xie, Zhihuang Tang, Caixian Microbiome Research BACKGROUND: Understanding how elevated atmospheric CO(2) (eCO(2)) impacts on phosphorus (P) transformation in plant rhizosphere is critical for maintaining ecological sustainability in response to climate change, especially in agricultural systems where soil P availability is low. METHODS: This study used rhizoboxes to physically separate rhizosphere regions (plant root-soil interface) into 1.5-mm segments. Wheat plants were grown in rhizoboxes under eCO(2) (800 ppm) and ambient CO(2) (400 ppm) in two farming soils, Chromosol and Vertosol, supplemented with phytate (organic P). Photosynthetic carbon flow in the plant-soil continuum was traced with (13)CO(2) labeling. Amplicon sequencing was performed on the rhizosphere-associated microbial community in the root-growth zone, and 1.5 mm and 3 mm away from the root. RESULTS: Elevated CO(2) accelerated the mineralization of phytate in the rhizosphere zones, which corresponded with increases in plant-derived (13)C enrichment and the relative abundances of discreet phylogenetic clades containing Bacteroidetes and Gemmatimonadetes in the bacterial community, and Funneliformis affiliated to arbuscular mycorrhizas in the fungal community. Although the amplicon sequence variants (ASVs) associated the stimulation of phytate mineralization under eCO(2) differed between the two soils, these ASVs belonged to the same phyla associated with phytase and phosphatase production. The symbiotic mycorrhizas in the rhizosphere of wheat under eCO(2) benefited from increased plant C supply and increased P access from soil. Further supportive evidence was the eCO(2)-induced increase in the genetic pool expressing the pentose phosphate pathway, which is the central pathway for biosynthesis of RNA/DNA precursors. CONCLUSIONS: The results suggested that an increased belowground carbon flow under eCO(2) stimulated bacterial growth, changing community composition in favor of phylotypes capable of degrading aromatic P compounds. It is proposed that energy investments by bacteria into anabolic processes increase under eCO(2) to level microbial P-use efficiencies and that synergies with symbiotic mycorrhizas further enhance the competition for and mineralization of organic P. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01203-w. BioMed Central 2022-01-24 /pmc/articles/PMC8785599/ /pubmed/35074003 http://dx.doi.org/10.1186/s40168-021-01203-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Jin, Jian
Krohn, Christian
Franks, Ashley E.
Wang, Xiaojuan
Wood, Jennifer L.
Petrovski, Steve
McCaskill, Malcolm
Batinovic, Steven
Xie, Zhihuang
Tang, Caixian
Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
title Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
title_full Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
title_fullStr Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
title_full_unstemmed Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
title_short Elevated atmospheric CO(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
title_sort elevated atmospheric co(2) alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8785599/
https://www.ncbi.nlm.nih.gov/pubmed/35074003
http://dx.doi.org/10.1186/s40168-021-01203-w
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