“Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres
ABSTRACT Archaea catalyzing the first step of nitrification in the rhizosphere possibly have an influence on plant growth and development. In this study, we found a distinct archaeal community, dominated by ammonia-oxidizing archaea (AOA), associated with the root system of pepper (Capsicum anuum L....
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| Language: | English |
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American Society for Microbiology
2024-12-01
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| Series: | mSphere |
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| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00821-24 |
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| author | Ui-Ju Lee Joo-Han Gwak Seungyeon Choi Man-Young Jung Tae Kwon Lee Hojin Ryu Samuel Imisi Awala Wolfgang Wanek Michael Wagner Zhe-Xue Quan Sung-Keun Rhee |
| author_facet | Ui-Ju Lee Joo-Han Gwak Seungyeon Choi Man-Young Jung Tae Kwon Lee Hojin Ryu Samuel Imisi Awala Wolfgang Wanek Michael Wagner Zhe-Xue Quan Sung-Keun Rhee |
| author_sort | Ui-Ju Lee |
| collection | DOAJ |
| description | ABSTRACT Archaea catalyzing the first step of nitrification in the rhizosphere possibly have an influence on plant growth and development. In this study, we found a distinct archaeal community, dominated by ammonia-oxidizing archaea (AOA), associated with the root system of pepper (Capsicum anuum L.) and ginseng plants (Panax ginseng C.A. Mey.) compared to bulk soil not penetrated by roots. While the abundance of total AOA decreased in the rhizosphere soils, AOA related to “Candidatus Nitrosocosmicus,” which harbor gene encoding manganese catalase (MnKat) in contrast to most other AOA, dominated the AOA community in the rhizosphere soils. For both plant species, the ratio of copy numbers of the AOA MnKat gene to the amoA gene (encoding the ammonia monooxygenase subunit A) was significantly higher in the rhizospheres than in bulk soils. In contrast to MnKat-negative strains from other AOA clades, the catalase activity of a representative isolate of “Ca. Nitrosocosmicus” was demonstrated. Members of this clade were enriched in H2O2-amended bulk soils, and constitutive expression of their MnKat gene was observed in both bulk and rhizosphere soils. Due to their abundance, “Ca. Nitrosocosmicus” members can be considered important players mediating the nitrification process in rhizospheres. The dominance of this MnKat-containing AOA in rhizospheres of agriculturally important plants hints at a previously overlooked AOA-plant interaction.IMPORTANCEAmmonia-oxidizing archaea (AOA) are widespread in terrestrial environments and outnumber other ammonia oxidizers in the rhizosphere, possibly exerting an influence on plant growth and development. However, little is known about the selection forces that shape their composition, functions, survival, and proliferation strategies in the rhizosphere. Here, we observed a distinct AOA community on root systems of two different plant species compared to bulk soil. Our results show that the “Ca. Nitrosocosmicus” clade, which possesses functional MnKat genes unlike most other AOA, dominated the rhizosphere soils. Moreover, members of this clade were enriched in H2O2-amended bulk soil, which mimics the ROS stress in root systems. While research on AOA-plant interactions in the rhizosphere is still in its infancy, these findings suggest that “Ca. Nitrosocosmicus” may be an important clade of AOA with potential AOA-plant interaction. |
| format | Article |
| id | doaj-art-7d10c4b9e2d348e3b03b924701a5da91 |
| institution | Kabale University |
| issn | 2379-5042 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj-art-7d10c4b9e2d348e3b03b924701a5da912024-12-19T14:00:33ZengAmerican Society for MicrobiologymSphere2379-50422024-12-0191210.1128/msphere.00821-24“Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheresUi-Ju Lee0Joo-Han Gwak1Seungyeon Choi2Man-Young Jung3Tae Kwon Lee4Hojin Ryu5Samuel Imisi Awala6Wolfgang Wanek7Michael Wagner8Zhe-Xue Quan9Sung-Keun Rhee10Department of Biological Sciences and Biotechnology, Chungbuk National University, Cheongju, Republic of KoreaDepartment of Biological Sciences and Biotechnology, Chungbuk National University, Cheongju, Republic of KoreaDepartment of Biological Sciences and Biotechnology, Chungbuk National University, Cheongju, Republic of KoreaDepartment of Science Education, Jeju National University, Jeju, Republic of KoreaDepartment of Environmental Engineering, Yonsei University, Wonju, Republic of KoreaDepartment of Biological Sciences and Biotechnology, Chungbuk National University, Cheongju, Republic of KoreaDepartment of Biological Sciences and Biotechnology, Chungbuk National University, Cheongju, Republic of KoreaDivision of Terrestrial Ecosystem Research, Center of Microbiology and Environmental Systems Science, University of Vienna, Vienna, AustriaDepartment of Microbiology and Ecosystem Science, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, AustriaSchool of Life Sciences, Fudan University, Shanghai, ChinaDepartment of Biological Sciences and Biotechnology, Chungbuk National University, Cheongju, Republic of KoreaABSTRACT Archaea catalyzing the first step of nitrification in the rhizosphere possibly have an influence on plant growth and development. In this study, we found a distinct archaeal community, dominated by ammonia-oxidizing archaea (AOA), associated with the root system of pepper (Capsicum anuum L.) and ginseng plants (Panax ginseng C.A. Mey.) compared to bulk soil not penetrated by roots. While the abundance of total AOA decreased in the rhizosphere soils, AOA related to “Candidatus Nitrosocosmicus,” which harbor gene encoding manganese catalase (MnKat) in contrast to most other AOA, dominated the AOA community in the rhizosphere soils. For both plant species, the ratio of copy numbers of the AOA MnKat gene to the amoA gene (encoding the ammonia monooxygenase subunit A) was significantly higher in the rhizospheres than in bulk soils. In contrast to MnKat-negative strains from other AOA clades, the catalase activity of a representative isolate of “Ca. Nitrosocosmicus” was demonstrated. Members of this clade were enriched in H2O2-amended bulk soils, and constitutive expression of their MnKat gene was observed in both bulk and rhizosphere soils. Due to their abundance, “Ca. Nitrosocosmicus” members can be considered important players mediating the nitrification process in rhizospheres. The dominance of this MnKat-containing AOA in rhizospheres of agriculturally important plants hints at a previously overlooked AOA-plant interaction.IMPORTANCEAmmonia-oxidizing archaea (AOA) are widespread in terrestrial environments and outnumber other ammonia oxidizers in the rhizosphere, possibly exerting an influence on plant growth and development. However, little is known about the selection forces that shape their composition, functions, survival, and proliferation strategies in the rhizosphere. Here, we observed a distinct AOA community on root systems of two different plant species compared to bulk soil. Our results show that the “Ca. Nitrosocosmicus” clade, which possesses functional MnKat genes unlike most other AOA, dominated the rhizosphere soils. Moreover, members of this clade were enriched in H2O2-amended bulk soil, which mimics the ROS stress in root systems. While research on AOA-plant interactions in the rhizosphere is still in its infancy, these findings suggest that “Ca. Nitrosocosmicus” may be an important clade of AOA with potential AOA-plant interaction.https://journals.asm.org/doi/10.1128/msphere.00821-24rhizosphereammonia-oxidizing archaeacatalasenitrification |
| spellingShingle | Ui-Ju Lee Joo-Han Gwak Seungyeon Choi Man-Young Jung Tae Kwon Lee Hojin Ryu Samuel Imisi Awala Wolfgang Wanek Michael Wagner Zhe-Xue Quan Sung-Keun Rhee “Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres mSphere rhizosphere ammonia-oxidizing archaea catalase nitrification |
| title | “Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres |
| title_full | “Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres |
| title_fullStr | “Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres |
| title_full_unstemmed | “Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres |
| title_short | “Ca. Nitrosocosmicus” members are the dominant archaea associated with plant rhizospheres |
| title_sort | ca nitrosocosmicus members are the dominant archaea associated with plant rhizospheres |
| topic | rhizosphere ammonia-oxidizing archaea catalase nitrification |
| url | https://journals.asm.org/doi/10.1128/msphere.00821-24 |
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