A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
The perennial gramineous grass <i>Miscanthus condensatus</i> functions as a major pioneer plant in colonizing acidic volcanic deposits on Miyake-jima, Japan, despite a lack of nitrogen nutrients. The nitrogen cycle in the rhizosphere is important for the vigorous growth of <i>M. co...
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MDPI AG
2023-01-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/11/2/260 |
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| author | Ahmad Arsyadi Yong Guo Akiko Ebihara Nobuo Sakagami Midori Sakoda Kanako Tago Takashi Kamijo Hiroyuki Ohta Tomoyasu Nishizawa |
| author_facet | Ahmad Arsyadi Yong Guo Akiko Ebihara Nobuo Sakagami Midori Sakoda Kanako Tago Takashi Kamijo Hiroyuki Ohta Tomoyasu Nishizawa |
| author_sort | Ahmad Arsyadi |
| collection | DOAJ |
| description | The perennial gramineous grass <i>Miscanthus condensatus</i> functions as a major pioneer plant in colonizing acidic volcanic deposits on Miyake-jima, Japan, despite a lack of nitrogen nutrients. The nitrogen cycle in the rhizosphere is important for the vigorous growth of <i>M. condensatus</i> in this unfavorable environment. In the present study, we identified the nitrogen-cycling bacterial community in the <i>M. condensatus</i> rhizosphere on these volcanic deposits using a combination of metagenomics and culture-based analyses. Our results showed a large number of functional genes related to denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in the rhizosphere, indicating that nitrate-transforming bacteria dominated the rhizosphere biome. Furthermore, nitrite reductase genes (i.e., <i>nirK</i> and <i>nirS</i>) related to the denitrification and those genes related to DNRA (i.e., <i>nirB</i> and <i>nrfA</i>) were mainly annotated to the classes Alpha-proteobacteria, Beta-proteobacteria, and Gamma-proteobacteria. A total of 304 nitrate-succinate-stimulated isolates were obtained from the <i>M. condensatus</i> rhizosphere and were classified into 34 operational taxonomic units according to amplified 16S rRNA gene restriction fragment pattern analysis. Additionally, two strains belonging to the genus <i>Cupriavidus</i> in the class Beta-proteobacteria showed a high in vitro denitrifying activity; however, metagenomic results indicated that the DNRA-related rhizobacteria appeared to take a major role in the nitrogen cycle of the <i>M. condensatus</i> rhizosphere in recent Miyake-jima volcanic deposits. This study elucidates the association between the <i>Miscanthus</i> rhizosphere and the nitrate-reducing bacterial community on newly placed volcanic deposits, which furthers our understanding of the transformation of nitrogen nutrition involved in the early development of vegetation. |
| first_indexed | 2024-03-11T08:24:11Z |
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| id | doaj.art-54c637eb2ae84f9aa47dfb5439bcce26 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-11T08:24:11Z |
| publishDate | 2023-01-01 |
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| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-54c637eb2ae84f9aa47dfb5439bcce262023-11-16T22:13:34ZengMDPI AGMicroorganisms2076-26072023-01-0111226010.3390/microorganisms11020260A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jimaAhmad Arsyadi0Yong Guo1Akiko Ebihara2Nobuo Sakagami3Midori Sakoda4Kanako Tago5Takashi Kamijo6Hiroyuki Ohta7Tomoyasu Nishizawa8Graduate School of Agriculture, Ibaraki University, Ibaraki 300-0393, JapanCollege of Agriculture, Ibaraki University, Ibaraki 300-0393, JapanGraduate School of Agriculture, Ibaraki University, Ibaraki 300-0393, JapanGraduate School of Agriculture, Ibaraki University, Ibaraki 300-0393, JapanUnited Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo 183-8509, JapanInstitute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8604, JapanFaculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki 305-8572, JapanGraduate School of Agriculture, Ibaraki University, Ibaraki 300-0393, JapanGraduate School of Agriculture, Ibaraki University, Ibaraki 300-0393, JapanThe perennial gramineous grass <i>Miscanthus condensatus</i> functions as a major pioneer plant in colonizing acidic volcanic deposits on Miyake-jima, Japan, despite a lack of nitrogen nutrients. The nitrogen cycle in the rhizosphere is important for the vigorous growth of <i>M. condensatus</i> in this unfavorable environment. In the present study, we identified the nitrogen-cycling bacterial community in the <i>M. condensatus</i> rhizosphere on these volcanic deposits using a combination of metagenomics and culture-based analyses. Our results showed a large number of functional genes related to denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in the rhizosphere, indicating that nitrate-transforming bacteria dominated the rhizosphere biome. Furthermore, nitrite reductase genes (i.e., <i>nirK</i> and <i>nirS</i>) related to the denitrification and those genes related to DNRA (i.e., <i>nirB</i> and <i>nrfA</i>) were mainly annotated to the classes Alpha-proteobacteria, Beta-proteobacteria, and Gamma-proteobacteria. A total of 304 nitrate-succinate-stimulated isolates were obtained from the <i>M. condensatus</i> rhizosphere and were classified into 34 operational taxonomic units according to amplified 16S rRNA gene restriction fragment pattern analysis. Additionally, two strains belonging to the genus <i>Cupriavidus</i> in the class Beta-proteobacteria showed a high in vitro denitrifying activity; however, metagenomic results indicated that the DNRA-related rhizobacteria appeared to take a major role in the nitrogen cycle of the <i>M. condensatus</i> rhizosphere in recent Miyake-jima volcanic deposits. This study elucidates the association between the <i>Miscanthus</i> rhizosphere and the nitrate-reducing bacterial community on newly placed volcanic deposits, which furthers our understanding of the transformation of nitrogen nutrition involved in the early development of vegetation.https://www.mdpi.com/2076-2607/11/2/260nitrate-reducing bacteriametagenomepioneer plantvolcanic depositsrhizosphere |
| spellingShingle | Ahmad Arsyadi Yong Guo Akiko Ebihara Nobuo Sakagami Midori Sakoda Kanako Tago Takashi Kamijo Hiroyuki Ohta Tomoyasu Nishizawa A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima Microorganisms nitrate-reducing bacteria metagenome pioneer plant volcanic deposits rhizosphere |
| title | A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima |
| title_full | A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima |
| title_fullStr | A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima |
| title_full_unstemmed | A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima |
| title_short | A Nitrate-Transforming Bacterial Community Dominates in the <i>Miscanthus</i> Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima |
| title_sort | nitrate transforming bacterial community dominates in the i miscanthus i rhizosphere on nitrogen deficient volcanic deposits of miyake jima |
| topic | nitrate-reducing bacteria metagenome pioneer plant volcanic deposits rhizosphere |
| url | https://www.mdpi.com/2076-2607/11/2/260 |
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