Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters

ABSTRACT Rice cultivation worldwide accounts for ∼7 to 17% of global methane emissions. Methane cycling in rice paddies is a microbial process not only involving methane producers (methanogens) and methane metabolizers (methanotrophs) but also other microbial taxa that affect upstream processes rela...

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Autores principales:	Zachary Liechty, Christian Santos-Medellín, Joseph Edwards, Bao Nguyen, David Mikhail, Shane Eason, Gregory Phillips, Venkatesan Sundaresan
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	endosphere fermentation methane methanogenesis microbiome rhizoplane Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2d96c757f9d14ec0ae0a56d403e6e68e
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spelling	oai:doaj.org-article:2d96c757f9d14ec0ae0a56d403e6e68e2021-12-02T19:46:18ZComparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters10.1128/mSystems.00897-192379-5077https://doaj.org/article/2d96c757f9d14ec0ae0a56d403e6e68e2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00897-19https://doaj.org/toc/2379-5077ABSTRACT Rice cultivation worldwide accounts for ∼7 to 17% of global methane emissions. Methane cycling in rice paddies is a microbial process not only involving methane producers (methanogens) and methane metabolizers (methanotrophs) but also other microbial taxa that affect upstream processes related to methane metabolism. Rice cultivars vary in their rates of methane emissions, but the influence of rice genotypes on methane cycling microbiota has been poorly characterized. Here, we profiled the rhizosphere, rhizoplane, and endosphere microbiomes of a high-methane-emitting cultivar (Sabine) and a low-methane-emitting cultivar (CLXL745) throughout the growing season to identify variations in the archaeal and bacterial communities relating to methane emissions. The rhizosphere of the high-emitting cultivar was enriched in methanogens compared to that in the low emitter, whereas the relative abundances of methanotrophs between the cultivars were not significantly different. Further analysis of cultivar-sensitive taxa identified families enriched in the high emitter that are associated with methanogenesis-related processes. The high emitter had greater relative abundances of sulfate-reducing and iron-reducing taxa which peak earlier in the season than methanogens and are necessary to lower soil oxidation reduction potential before methanogenesis can occur. The high emitter also had a greater abundance of fermentative taxa which produce methanogenesis precursors (acetate, CO2, and H2). Furthermore, the high emitter was enriched in taxa related to acetogenesis which compete with methanogens for CO2 and H2. These taxa were enriched in a spatio-specific manner and reveal a complex network of microbial interactions on which plant genotype-dependent factors can act to affect methanogenesis and methane emissions. IMPORTANCE Rice cultivation is a major source of anthropogenic emissions of methane, a greenhouse gas with a potentially severe impact on climate change. Emission variation between rice cultivars suggests the feasibility of breeding low-emission rice, but there is a limited understanding of how genotypes affect the microbiota involved in methane cycling. Here, we show that the root microbiome of the high-emitting cultivar is enriched both in methanogens and in taxa associated with fermentation, iron, and sulfate reduction and acetogenesis, processes that support methanogenesis. Understanding how cultivars affect microbes with methanogenesis-related functions is vital for understanding the genetic basis for methane emission in rice and can aid in the development of breeding programs that reduce the environmental impact of rice cultivation.Zachary LiechtyChristian Santos-MedellínJoseph EdwardsBao NguyenDavid MikhailShane EasonGregory PhillipsVenkatesan SundaresanAmerican Society for MicrobiologyarticleendospherefermentationmethanemethanogenesismicrobiomerhizoplaneMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	endosphere fermentation methane methanogenesis microbiome rhizoplane Microbiology QR1-502
spellingShingle	endosphere fermentation methane methanogenesis microbiome rhizoplane Microbiology QR1-502 Zachary Liechty Christian Santos-Medellín Joseph Edwards Bao Nguyen David Mikhail Shane Eason Gregory Phillips Venkatesan Sundaresan Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters
description	ABSTRACT Rice cultivation worldwide accounts for ∼7 to 17% of global methane emissions. Methane cycling in rice paddies is a microbial process not only involving methane producers (methanogens) and methane metabolizers (methanotrophs) but also other microbial taxa that affect upstream processes related to methane metabolism. Rice cultivars vary in their rates of methane emissions, but the influence of rice genotypes on methane cycling microbiota has been poorly characterized. Here, we profiled the rhizosphere, rhizoplane, and endosphere microbiomes of a high-methane-emitting cultivar (Sabine) and a low-methane-emitting cultivar (CLXL745) throughout the growing season to identify variations in the archaeal and bacterial communities relating to methane emissions. The rhizosphere of the high-emitting cultivar was enriched in methanogens compared to that in the low emitter, whereas the relative abundances of methanotrophs between the cultivars were not significantly different. Further analysis of cultivar-sensitive taxa identified families enriched in the high emitter that are associated with methanogenesis-related processes. The high emitter had greater relative abundances of sulfate-reducing and iron-reducing taxa which peak earlier in the season than methanogens and are necessary to lower soil oxidation reduction potential before methanogenesis can occur. The high emitter also had a greater abundance of fermentative taxa which produce methanogenesis precursors (acetate, CO2, and H2). Furthermore, the high emitter was enriched in taxa related to acetogenesis which compete with methanogens for CO2 and H2. These taxa were enriched in a spatio-specific manner and reveal a complex network of microbial interactions on which plant genotype-dependent factors can act to affect methanogenesis and methane emissions. IMPORTANCE Rice cultivation is a major source of anthropogenic emissions of methane, a greenhouse gas with a potentially severe impact on climate change. Emission variation between rice cultivars suggests the feasibility of breeding low-emission rice, but there is a limited understanding of how genotypes affect the microbiota involved in methane cycling. Here, we show that the root microbiome of the high-emitting cultivar is enriched both in methanogens and in taxa associated with fermentation, iron, and sulfate reduction and acetogenesis, processes that support methanogenesis. Understanding how cultivars affect microbes with methanogenesis-related functions is vital for understanding the genetic basis for methane emission in rice and can aid in the development of breeding programs that reduce the environmental impact of rice cultivation.
format	article
author	Zachary Liechty Christian Santos-Medellín Joseph Edwards Bao Nguyen David Mikhail Shane Eason Gregory Phillips Venkatesan Sundaresan
author_facet	Zachary Liechty Christian Santos-Medellín Joseph Edwards Bao Nguyen David Mikhail Shane Eason Gregory Phillips Venkatesan Sundaresan
author_sort	Zachary Liechty
title	Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters
title_short	Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters
title_full	Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters
title_fullStr	Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters
title_full_unstemmed	Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters
title_sort	comparative analysis of root microbiomes of rice cultivars with high and low methane emissions reveals differences in abundance of methanogenic archaea and putative upstream fermenters
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2d96c757f9d14ec0ae0a56d403e6e68e
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Comparative Analysis of Root Microbiomes of Rice Cultivars with High and Low Methane Emissions Reveals Differences in Abundance of Methanogenic Archaea and Putative Upstream Fermenters

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