Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano
Terrestrial mud volcanoes (MVs) are an important natural source of methane emission. The role of microbial processes in methane cycling and organic transformation in such environments remains largely unexplored. In this study, we aim to uncover functional potentials and community assemblages across...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2017-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02137/full |
| _version_ | 1811342922405117952 |
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| author | Tzu-Hsuan Tu Tzu-Hsuan Tu Tzu-Hsuan Tu Li-Wei Wu Li-Wei Wu Yu-Shih Lin Hiroyuki Imachi Hiroyuki Imachi Li-Hung Lin Pei-Ling Wang |
| author_facet | Tzu-Hsuan Tu Tzu-Hsuan Tu Tzu-Hsuan Tu Li-Wei Wu Li-Wei Wu Yu-Shih Lin Hiroyuki Imachi Hiroyuki Imachi Li-Hung Lin Pei-Ling Wang |
| author_sort | Tzu-Hsuan Tu |
| collection | DOAJ |
| description | Terrestrial mud volcanoes (MVs) are an important natural source of methane emission. The role of microbial processes in methane cycling and organic transformation in such environments remains largely unexplored. In this study, we aim to uncover functional potentials and community assemblages across geochemical transitions in a ferruginous, sulfate-depleted MV of eastern Taiwan. Geochemical profiles combined with 16S rRNA gene abundances indicated that anaerobic oxidation of methane (AOM) mediated by ANME-2a group coincided with iron/manganese reduction by Desulfuromonadales at shallow depths deprived of sulfate. The activity of AOM was stimulated either by methane alone or by methane and a range of electron acceptors, such as sulfate, ferrihydrite, and artificial humic acid. Metagenomic analyses revealed that functional genes for AOM and metal reduction were more abundant at shallow intervals. In particular, genes encoding pili expression and electron transport through multi-heme cytochromes were prevalent, suggesting potential intercellular interactions for electron transport involved in AOM. For comparison, genes responsible for methanogenesis and degradation of chitin and plant-derived molecules were more abundant at depth. The gene distribution combined with the enhanced proportions of 16S rRNA genes related to methanogens and heterotrophs, and geochemical characteristics suggest that particulate organic matter was degraded into various organic entities that could further fuel in situ methanogenesis. Finally, genes responsible for aerobic methane oxidation were more abundant in the bubbling pool and near-surface sediments. These methane oxidizers account for the ultimate attenuation of methane discharge into the atmosphere. Overall, our results demonstrated that various community members were compartmentalized into stratified niches along geochemical gradients. These community members form a metabolic network that cascades the carbon transformation from the upstream degradation of recalcitrant organic carbon with fermentative production of labile organic entities and methane to downstream methane oxidation and metal reduction near the surface. Such a metabolic architecture enables effective methane removal under ferruginous, sulfate-depleted conditions in terrestrial MVs. |
| first_indexed | 2024-04-13T19:20:37Z |
| format | Article |
| id | doaj.art-bf7b0a66965a4d0b8820e64d1094cf4b |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T19:20:37Z |
| publishDate | 2017-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-bf7b0a66965a4d0b8820e64d1094cf4b2022-12-22T02:33:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-11-01810.3389/fmicb.2017.02137286980Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud VolcanoTzu-Hsuan Tu0Tzu-Hsuan Tu1Tzu-Hsuan Tu2Li-Wei Wu3Li-Wei Wu4Yu-Shih Lin5Hiroyuki Imachi6Hiroyuki Imachi7Li-Hung Lin8Pei-Ling Wang9Institute of Oceanography, National Taiwan University, Taipei, TaiwanDepartment of Geosciences, National Taiwan University, Taipei, TaiwanDepartment of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology, Yokosuka, JapanDepartment of Geosciences, National Taiwan University, Taipei, TaiwanThe Experimental Forest, College of Bio-Resources and Agriculture, National Taiwan University, Nantou, TaiwanDepartment of Oceanography, National Sun Yat-sen University, Kaohsiung, TaiwanDepartment of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology, Yokosuka, JapanResearch and Development Center for Marine Resources, Japan Agency for Marine-Earth Science and Technology, Yokosuka, JapanDepartment of Geosciences, National Taiwan University, Taipei, TaiwanInstitute of Oceanography, National Taiwan University, Taipei, TaiwanTerrestrial mud volcanoes (MVs) are an important natural source of methane emission. The role of microbial processes in methane cycling and organic transformation in such environments remains largely unexplored. In this study, we aim to uncover functional potentials and community assemblages across geochemical transitions in a ferruginous, sulfate-depleted MV of eastern Taiwan. Geochemical profiles combined with 16S rRNA gene abundances indicated that anaerobic oxidation of methane (AOM) mediated by ANME-2a group coincided with iron/manganese reduction by Desulfuromonadales at shallow depths deprived of sulfate. The activity of AOM was stimulated either by methane alone or by methane and a range of electron acceptors, such as sulfate, ferrihydrite, and artificial humic acid. Metagenomic analyses revealed that functional genes for AOM and metal reduction were more abundant at shallow intervals. In particular, genes encoding pili expression and electron transport through multi-heme cytochromes were prevalent, suggesting potential intercellular interactions for electron transport involved in AOM. For comparison, genes responsible for methanogenesis and degradation of chitin and plant-derived molecules were more abundant at depth. The gene distribution combined with the enhanced proportions of 16S rRNA genes related to methanogens and heterotrophs, and geochemical characteristics suggest that particulate organic matter was degraded into various organic entities that could further fuel in situ methanogenesis. Finally, genes responsible for aerobic methane oxidation were more abundant in the bubbling pool and near-surface sediments. These methane oxidizers account for the ultimate attenuation of methane discharge into the atmosphere. Overall, our results demonstrated that various community members were compartmentalized into stratified niches along geochemical gradients. These community members form a metabolic network that cascades the carbon transformation from the upstream degradation of recalcitrant organic carbon with fermentative production of labile organic entities and methane to downstream methane oxidation and metal reduction near the surface. Such a metabolic architecture enables effective methane removal under ferruginous, sulfate-depleted conditions in terrestrial MVs.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02137/fullmud volcanomethaneAOMmethanogenesisANMETaiwan |
| spellingShingle | Tzu-Hsuan Tu Tzu-Hsuan Tu Tzu-Hsuan Tu Li-Wei Wu Li-Wei Wu Yu-Shih Lin Hiroyuki Imachi Hiroyuki Imachi Li-Hung Lin Pei-Ling Wang Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano Frontiers in Microbiology mud volcano methane AOM methanogenesis ANME Taiwan |
| title | Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano |
| title_full | Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano |
| title_fullStr | Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano |
| title_full_unstemmed | Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano |
| title_short | Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano |
| title_sort | microbial community composition and functional capacity in a terrestrial ferruginous sulfate depleted mud volcano |
| topic | mud volcano methane AOM methanogenesis ANME Taiwan |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02137/full |
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