Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions

Rice paddies are major contributors to anthropogenic greenhouse gas emissions via methane (CH4) flux. The accurate quantification of CH4 emissions from rice paddies remains problematic, in part due to uncertainties and omissions in the contribution of microbial aggregates on the soil surface to carb...

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Main Authors: Sichu Wang, Pengfei Sun, Guangbin Zhang, Neil Gray, Jan Dolfing, Sofia Esquivel-Elizondo, Josep Peñuelas, Yonghong Wu
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:The Innovation
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S266667582100117X
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author Sichu Wang
Pengfei Sun
Guangbin Zhang
Neil Gray
Jan Dolfing
Sofia Esquivel-Elizondo
Josep Peñuelas
Yonghong Wu
author_facet Sichu Wang
Pengfei Sun
Guangbin Zhang
Neil Gray
Jan Dolfing
Sofia Esquivel-Elizondo
Josep Peñuelas
Yonghong Wu
author_sort Sichu Wang
collection DOAJ
description Rice paddies are major contributors to anthropogenic greenhouse gas emissions via methane (CH4) flux. The accurate quantification of CH4 emissions from rice paddies remains problematic, in part due to uncertainties and omissions in the contribution of microbial aggregates on the soil surface to carbon fluxes. Herein, we comprehensively evaluated the contribution of one form of microbial aggregates, periphytic biofilm (PB), to carbon dioxide (CO2) and CH4 emissions from paddies distributed across three climatic zones, and quantified the pathways that drive net CH4 production as well as CO2 fixation. We found that PB accounted for 7.1%–38.5% of CH4 emissions and 7.2%–12.7% of CO2 fixation in the rice paddies. During their growth phase, PB fixed CO2 and increased the redox potential, which promoted aerobic CH4 oxidation. During the decay phase, PB degradation reduced redox potential and increased soil organic carbon availability, which promoted methanogenic microbial community growth and metabolism and increased CH4 emissions. Overall, PB acted as a biotic converter of atmospheric CO2 to CH4, and aggravated carbon emissions by up to 2,318 kg CO2 equiv ha−1 season−1. Our results provide proof-of-concept evidence for the discrimination of the contributions of surface microbial aggregates (i.e., PB) from soil microbes, and a profound foundation for the estimation and simulation of carbon fluxes in a potential novel approach to the mitigation of CH4 emissions by manipulating PB growth. Public summary: • Field experiments were conducted in tropical, subtropical, and temperate rice paddies • Periphytic biofilm promoted CO2 fixation and CH4 emission • Periphytic biofilm acted as a biotic converter of atmospheric CO2 to CH4
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spelling doaj.art-b67dfb4cd59f436c896cb4e547938de52022-12-22T04:10:18ZengElsevierThe Innovation2666-67582022-01-0131100192Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissionsSichu Wang0Pengfei Sun1Guangbin Zhang2Neil Gray3Jan Dolfing4Sofia Esquivel-Elizondo5Josep Peñuelas6Yonghong Wu7State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, China; Zigui Three Gorges Reservoir Ecosystem, Observation and Research Station of Ministry of Water Resources of the People's Republic of China, Shuitianba Zigui, Yichang 443605, China; College of Advanced Agricultural Science, University of Chinese Academy of Sciences, No. 19(A) Yuquan Road, Shijingshan District, Beijing 100049, ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, China; Zigui Three Gorges Reservoir Ecosystem, Observation and Research Station of Ministry of Water Resources of the People's Republic of China, Shuitianba Zigui, Yichang 443605, ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, ChinaSchool of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne NE1 7RU, UKFaculty of Energy and Environment, Northumbria University, Newcastle upon Tyne NE1 8QH, UKDepartment of Microbiome Science, Max Planck Institute for Developmental Biology, Max-Planck-Ring 5, 72076 Tübingen, GermanyConsejo Superior de Investigaciones Científicas (CSIC), Global Ecology Unit, Centre for Ecological Research and Forestry Applications (CREAF)–CSIC–Universitat Autonoma de Barcelona (UAB), Bellaterra, 08193 Barcelona, Catalonia, SpainState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, China; Zigui Three Gorges Reservoir Ecosystem, Observation and Research Station of Ministry of Water Resources of the People's Republic of China, Shuitianba Zigui, Yichang 443605, China; Corresponding authorRice paddies are major contributors to anthropogenic greenhouse gas emissions via methane (CH4) flux. The accurate quantification of CH4 emissions from rice paddies remains problematic, in part due to uncertainties and omissions in the contribution of microbial aggregates on the soil surface to carbon fluxes. Herein, we comprehensively evaluated the contribution of one form of microbial aggregates, periphytic biofilm (PB), to carbon dioxide (CO2) and CH4 emissions from paddies distributed across three climatic zones, and quantified the pathways that drive net CH4 production as well as CO2 fixation. We found that PB accounted for 7.1%–38.5% of CH4 emissions and 7.2%–12.7% of CO2 fixation in the rice paddies. During their growth phase, PB fixed CO2 and increased the redox potential, which promoted aerobic CH4 oxidation. During the decay phase, PB degradation reduced redox potential and increased soil organic carbon availability, which promoted methanogenic microbial community growth and metabolism and increased CH4 emissions. Overall, PB acted as a biotic converter of atmospheric CO2 to CH4, and aggravated carbon emissions by up to 2,318 kg CO2 equiv ha−1 season−1. Our results provide proof-of-concept evidence for the discrimination of the contributions of surface microbial aggregates (i.e., PB) from soil microbes, and a profound foundation for the estimation and simulation of carbon fluxes in a potential novel approach to the mitigation of CH4 emissions by manipulating PB growth. Public summary: • Field experiments were conducted in tropical, subtropical, and temperate rice paddies • Periphytic biofilm promoted CO2 fixation and CH4 emission • Periphytic biofilm acted as a biotic converter of atmospheric CO2 to CH4http://www.sciencedirect.com/science/article/pii/S266667582100117Xperiphytic biofilmrice paddygreenhouse gas emissionscarbon fluxesredox potential
spellingShingle Sichu Wang
Pengfei Sun
Guangbin Zhang
Neil Gray
Jan Dolfing
Sofia Esquivel-Elizondo
Josep Peñuelas
Yonghong Wu
Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
The Innovation
periphytic biofilm
rice paddy
greenhouse gas emissions
carbon fluxes
redox potential
title Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
title_full Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
title_fullStr Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
title_full_unstemmed Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
title_short Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
title_sort contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions
topic periphytic biofilm
rice paddy
greenhouse gas emissions
carbon fluxes
redox potential
url http://www.sciencedirect.com/science/article/pii/S266667582100117X
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