TY - JOUR

T1 - Methanotrophy-driven accumulation of organic carbon in four paddy soils of Bangladesh

AU - Sultanta, Nasrin

AU - ZHAO, Jun

AU - Cai, Yuanfeng

AU - RAHMAN, G. K.M.Mustafizur

AU - ALAM, Mohammad Saiful

AU - FAHEEM, Mohammad

AU - Ho, Adrian

AU - JIA, Zhongjun

N1 - Funding Information: This study was financially supported by the National Natural Science Foundation of China (Nos. 91751204, 41630862, 41701302, 41530857, and 41877062). The first author, Ms. Nasrin Sultana, gratefully acknowledges the Organization for Women in Science for the Developing World (OWSD) Ph.D. Fellowship. The authors thank Mr. Zhiying Guo at Soil Sub-center of Chinese Ecological Research Network, Institute of Soil Science, Chinese Academy of Sciences (CAS) for bioinformatic analysis. We also thank the staff of the Analysis Center at the Institute of Soil Science, CAS for technical support, including Ms. Rong Huang and Mr. Zuohao Ma for Illumina MiSeq sequencing, Ms. Deling Sun for 13C-atom abundance assay, Ms. Yufang Sun for soil organic carbon and total nitrogen content assay, Mr. Ruhai Wang for ammonia and nitrate nitrogen content assays, and Mr. Guoxing Lu for soil organic matter assay.

PY - 2022/4

Y1 - 2022/4

N2 - Biological methane oxidation is a crucial process in the global carbon cycle that reduces methane emissions from paddy fields and natural wetlands into the atmosphere. However, soil organic carbon accumulation associated with microbial methane oxidation is poorly understood. Therefore, to investigate methane-derived carbon incorporation into soil organic matter, paddy soils originated from different parent materials (Inceptisol, Entisol, and Alfisol) were collected after rice harvesting from four major rice-producing regions in Bangladesh. Following microcosm incubation with 5% (volume/volume) 13CH2, soil 13C-atom abundances significantly increased from background level of 1.08% to 1.88%–2.78%, leading to a net methane-derived accumulation of soil organic carbon ranging from 120 to 307 mg kg-1. Approximately 23.6%–60.0% of the methane consumed was converted to soil organic carbon during microbial methane oxidation. The phylogeny of 13C-labeled pmoA (enconding the alpha subunit of the particulate methane monooxygenase) and 16S rRNA genes further revealed that canonical α (type II) and γ (type I) Proteobacteria were active methane oxidizers. Members within the Methylobacter- and Methylosarcina-affiliated type Ia lineages dominated active methane-oxidizing communities that were responsible for the majority of methane-derived carbon accumulation in all three paddy soils, while Methylocystis-affiliated type IIa lineage was the key contributor in one paddy soil of Inceptisol origin. These results suggest that methanotroph-mediated synthesis of biomass plays an important role in soil organic matter accumulation. This study thus supports the concept that methanotrophs not only consume the greenhouse gas methane but also serve as a key biotic factor in maintaining soil fertility.

AB - Biological methane oxidation is a crucial process in the global carbon cycle that reduces methane emissions from paddy fields and natural wetlands into the atmosphere. However, soil organic carbon accumulation associated with microbial methane oxidation is poorly understood. Therefore, to investigate methane-derived carbon incorporation into soil organic matter, paddy soils originated from different parent materials (Inceptisol, Entisol, and Alfisol) were collected after rice harvesting from four major rice-producing regions in Bangladesh. Following microcosm incubation with 5% (volume/volume) 13CH2, soil 13C-atom abundances significantly increased from background level of 1.08% to 1.88%–2.78%, leading to a net methane-derived accumulation of soil organic carbon ranging from 120 to 307 mg kg-1. Approximately 23.6%–60.0% of the methane consumed was converted to soil organic carbon during microbial methane oxidation. The phylogeny of 13C-labeled pmoA (enconding the alpha subunit of the particulate methane monooxygenase) and 16S rRNA genes further revealed that canonical α (type II) and γ (type I) Proteobacteria were active methane oxidizers. Members within the Methylobacter- and Methylosarcina-affiliated type Ia lineages dominated active methane-oxidizing communities that were responsible for the majority of methane-derived carbon accumulation in all three paddy soils, while Methylocystis-affiliated type IIa lineage was the key contributor in one paddy soil of Inceptisol origin. These results suggest that methanotroph-mediated synthesis of biomass plays an important role in soil organic matter accumulation. This study thus supports the concept that methanotrophs not only consume the greenhouse gas methane but also serve as a key biotic factor in maintaining soil fertility.

KW - 16S rRNA gene

KW - DNA-based stable-isotope probing (DNA-SIP)

KW - methane oxidation

KW - methanotroph

KW - pmoA

KW - rice soil

KW - soil organic carbon

KW - soil organic matter

UR - http://www.scopus.com/inward/record.url?scp=85121710069&partnerID=8YFLogxK

U2 - 10.1016/S1002-0160(20)60030-3

DO - 10.1016/S1002-0160(20)60030-3

M3 - Article

AN - SCOPUS:85121710069

VL - 32

SP - 348

EP - 358

JO - PEDOSPHERE

JF - PEDOSPHERE

SN - 1002-0160

IS - 2

ER -