Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes
Abstract Background Mangrove ecosystems are considered as hot spots of biogeochemical cycling, yet the diversity, function and coupling mechanism of microbially driven biogeochemical cycling along the sediment depth of mangrove wetlands remain elusive. Here we investigated the vertical profile of me...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-04-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01501-5 |
| _version_ | 1797849949070688256 |
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| author | Lu Qian Xiaoli Yu Hang Gu Fei Liu Yijun Fan Cheng Wang Qiang He Yun Tian Yisheng Peng Longfei Shu Shanquan Wang Zhijian Huang Qingyun Yan Jianguo He Guangli Liu Qichao Tu Zhili He |
| author_facet | Lu Qian Xiaoli Yu Hang Gu Fei Liu Yijun Fan Cheng Wang Qiang He Yun Tian Yisheng Peng Longfei Shu Shanquan Wang Zhijian Huang Qingyun Yan Jianguo He Guangli Liu Qichao Tu Zhili He |
| author_sort | Lu Qian |
| collection | DOAJ |
| description | Abstract Background Mangrove ecosystems are considered as hot spots of biogeochemical cycling, yet the diversity, function and coupling mechanism of microbially driven biogeochemical cycling along the sediment depth of mangrove wetlands remain elusive. Here we investigated the vertical profile of methane (CH4), nitrogen (N) and sulphur (S) cycling genes/pathways and their potential coupling mechanisms using metagenome sequencing approaches. Results Our results showed that the metabolic pathways involved in CH4, N and S cycling were mainly shaped by pH and acid volatile sulphide (AVS) along a sediment depth, and AVS was a critical electron donor impacting mangrove sediment S oxidation and denitrification. Gene families involved in S oxidation and denitrification significantly (P < 0.05) decreased along the sediment depth and could be coupled by S-driven denitrifiers, such as Burkholderiaceae and Sulfurifustis in the surface sediment (0–15 cm). Interestingly, all S-driven denitrifier metagenome-assembled genomes (MAGs) appeared to be incomplete denitrifiers with nitrate/nitrite/nitric oxide reductases (Nar/Nir/Nor) but without nitrous oxide reductase (Nos), suggesting such sulphide-utilizing groups might be an important contributor to N2O production in the surface mangrove sediment. Gene families involved in methanogenesis and S reduction significantly (P < 0.05) increased along the sediment depth. Based on both network and MAG analyses, sulphate-reducing bacteria (SRB) might develop syntrophic relationships with anaerobic CH4 oxidizers (ANMEs) by direct electron transfer or zero-valent sulphur, which would pull forward the co-existence of methanogens and SRB in the middle and deep layer sediments. Conclusions In addition to offering a perspective on the vertical distribution of microbially driven CH4, N and S cycling genes/pathways, this study emphasizes the important role of S-driven denitrifiers on N2O emissions and various possible coupling mechanisms of ANMEs and SRB along the mangrove sediment depth. The exploration of potential coupling mechanisms provides novel insights into future synthetic microbial community construction and analysis. This study also has important implications for predicting ecosystem functions within the context of environmental and global change. Video Abstract |
| first_indexed | 2024-04-09T18:52:27Z |
| format | Article |
| id | doaj.art-1dd197df3c134952b1a302551ab3f352 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-09T18:52:27Z |
| publishDate | 2023-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-1dd197df3c134952b1a302551ab3f3522023-04-09T11:22:25ZengBMCMicrobiome2049-26182023-04-0111111910.1186/s40168-023-01501-5Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomesLu Qian0Xiaoli Yu1Hang Gu2Fei Liu3Yijun Fan4Cheng Wang5Qiang He6Yun Tian7Yisheng Peng8Longfei Shu9Shanquan Wang10Zhijian Huang11Qingyun Yan12Jianguo He13Guangli Liu14Qichao Tu15Zhili He16Environmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityDepartment of Civil and Environmental Engineering, the University of TennesseeKey Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, School of Life Sciences, Xiamen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversitySchool of Marine Science, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversitySchool of Life Science, Sun Yat-Sen UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityInstitute of Marine Science and Technology, Shandong UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen UniversityAbstract Background Mangrove ecosystems are considered as hot spots of biogeochemical cycling, yet the diversity, function and coupling mechanism of microbially driven biogeochemical cycling along the sediment depth of mangrove wetlands remain elusive. Here we investigated the vertical profile of methane (CH4), nitrogen (N) and sulphur (S) cycling genes/pathways and their potential coupling mechanisms using metagenome sequencing approaches. Results Our results showed that the metabolic pathways involved in CH4, N and S cycling were mainly shaped by pH and acid volatile sulphide (AVS) along a sediment depth, and AVS was a critical electron donor impacting mangrove sediment S oxidation and denitrification. Gene families involved in S oxidation and denitrification significantly (P < 0.05) decreased along the sediment depth and could be coupled by S-driven denitrifiers, such as Burkholderiaceae and Sulfurifustis in the surface sediment (0–15 cm). Interestingly, all S-driven denitrifier metagenome-assembled genomes (MAGs) appeared to be incomplete denitrifiers with nitrate/nitrite/nitric oxide reductases (Nar/Nir/Nor) but without nitrous oxide reductase (Nos), suggesting such sulphide-utilizing groups might be an important contributor to N2O production in the surface mangrove sediment. Gene families involved in methanogenesis and S reduction significantly (P < 0.05) increased along the sediment depth. Based on both network and MAG analyses, sulphate-reducing bacteria (SRB) might develop syntrophic relationships with anaerobic CH4 oxidizers (ANMEs) by direct electron transfer or zero-valent sulphur, which would pull forward the co-existence of methanogens and SRB in the middle and deep layer sediments. Conclusions In addition to offering a perspective on the vertical distribution of microbially driven CH4, N and S cycling genes/pathways, this study emphasizes the important role of S-driven denitrifiers on N2O emissions and various possible coupling mechanisms of ANMEs and SRB along the mangrove sediment depth. The exploration of potential coupling mechanisms provides novel insights into future synthetic microbial community construction and analysis. This study also has important implications for predicting ecosystem functions within the context of environmental and global change. Video Abstracthttps://doi.org/10.1186/s40168-023-01501-5Vertical distributionMetagenome sequencing analysisMangrove sedimentMethane/nitrogen/sulphur cyclingMetagenome-assembled genomeCoupling mechanism |
| spellingShingle | Lu Qian Xiaoli Yu Hang Gu Fei Liu Yijun Fan Cheng Wang Qiang He Yun Tian Yisheng Peng Longfei Shu Shanquan Wang Zhijian Huang Qingyun Yan Jianguo He Guangli Liu Qichao Tu Zhili He Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes Microbiome Vertical distribution Metagenome sequencing analysis Mangrove sediment Methane/nitrogen/sulphur cycling Metagenome-assembled genome Coupling mechanism |
| title | Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes |
| title_full | Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes |
| title_fullStr | Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes |
| title_full_unstemmed | Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes |
| title_short | Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes |
| title_sort | vertically stratified methane nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes |
| topic | Vertical distribution Metagenome sequencing analysis Mangrove sediment Methane/nitrogen/sulphur cycling Metagenome-assembled genome Coupling mechanism |
| url | https://doi.org/10.1186/s40168-023-01501-5 |
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