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A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima

The perennial gramineous grass Miscanthus condensatus 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 M. condensatus in this unfavorabl...

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Autores principales: Arsyadi, Ahmad, Guo, Yong, Ebihara, Akiko, Sakagami, Nobuo, Sakoda, Midori, Tago, Kanako, Kamijo, Takashi, Ohta, Hiroyuki, Nishizawa, Tomoyasu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9961740/
https://www.ncbi.nlm.nih.gov/pubmed/36838234
http://dx.doi.org/10.3390/microorganisms11020260
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author Arsyadi, Ahmad
Guo, Yong
Ebihara, Akiko
Sakagami, Nobuo
Sakoda, Midori
Tago, Kanako
Kamijo, Takashi
Ohta, Hiroyuki
Nishizawa, Tomoyasu
author_facet Arsyadi, Ahmad
Guo, Yong
Ebihara, Akiko
Sakagami, Nobuo
Sakoda, Midori
Tago, Kanako
Kamijo, Takashi
Ohta, Hiroyuki
Nishizawa, Tomoyasu
author_sort Arsyadi, Ahmad
collection PubMed
description The perennial gramineous grass Miscanthus condensatus 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 M. condensatus in this unfavorable environment. In the present study, we identified the nitrogen-cycling bacterial community in the M. condensatus 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., nirK and nirS) related to the denitrification and those genes related to DNRA (i.e., nirB and nrfA) 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 M. condensatus 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 Cupriavidus 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 M. condensatus rhizosphere in recent Miyake-jima volcanic deposits. This study elucidates the association between the Miscanthus 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.
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spelling pubmed-99617402023-02-26 A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima Arsyadi, Ahmad Guo, Yong Ebihara, Akiko Sakagami, Nobuo Sakoda, Midori Tago, Kanako Kamijo, Takashi Ohta, Hiroyuki Nishizawa, Tomoyasu Microorganisms Article The perennial gramineous grass Miscanthus condensatus 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 M. condensatus in this unfavorable environment. In the present study, we identified the nitrogen-cycling bacterial community in the M. condensatus 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., nirK and nirS) related to the denitrification and those genes related to DNRA (i.e., nirB and nrfA) 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 M. condensatus 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 Cupriavidus 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 M. condensatus rhizosphere in recent Miyake-jima volcanic deposits. This study elucidates the association between the Miscanthus 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. MDPI 2023-01-19 /pmc/articles/PMC9961740/ /pubmed/36838234 http://dx.doi.org/10.3390/microorganisms11020260 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Arsyadi, Ahmad
Guo, Yong
Ebihara, Akiko
Sakagami, Nobuo
Sakoda, Midori
Tago, Kanako
Kamijo, Takashi
Ohta, Hiroyuki
Nishizawa, Tomoyasu
A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
title A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
title_full A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
title_fullStr A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
title_full_unstemmed A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
title_short A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima
title_sort nitrate-transforming bacterial community dominates in the miscanthus rhizosphere on nitrogen-deficient volcanic deposits of miyake-jima
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9961740/
https://www.ncbi.nlm.nih.gov/pubmed/36838234
http://dx.doi.org/10.3390/microorganisms11020260
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