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Volume 11
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10.3390/microorganisms11020260
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Article

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

by
Ahmad Arsyadi
1,†,
Yong Guo
2,*,
Akiko Ebihara
1,
Nobuo Sakagami
1,2,
Midori Sakoda
3,
Kanako Tago
4,
Takashi Kamijo
5,
Hiroyuki Ohta
1,2 and
Tomoyasu Nishizawa
1,2,3,*
1
Graduate School of Agriculture, Ibaraki University, Ibaraki 300-0393, Japan
2
College of Agriculture, Ibaraki University, Ibaraki 300-0393, Japan
3
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo 183-8509, Japan
4
Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8604, Japan
5
Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki 305-8572, Japan
*
Authors to whom correspondence should be addressed.
†
Current address: Department of Biology, Faculty of Agriculture, Fisheries and Biology, University of Bangka Belitung, Merawang 33172, Indonesia.
Microorganisms 2023, 11(2), 260; https://doi.org/10.3390/microorganisms11020260
Submission received: 30 November 2022 / Revised: 24 December 2022 / Accepted: 16 January 2023 / Published: 19 January 2023
(This article belongs to the Topic Plant-Associated Microbiota: From the Assembly to the Function)
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Abstract

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.
Keywords: nitrate-reducing bacteria; metagenome; pioneer plant; volcanic deposits; rhizosphere nitrate-reducing bacteria; metagenome; pioneer plant; volcanic deposits; rhizosphere

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MDPI and ACS Style

Arsyadi, A.; Guo, Y.; Ebihara, A.; Sakagami, N.; Sakoda, M.; Tago, K.; Kamijo, T.; Ohta, H.; Nishizawa, T. A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima. Microorganisms 2023, 11, 260. https://doi.org/10.3390/microorganisms11020260

AMA Style

Arsyadi A, Guo Y, Ebihara A, Sakagami N, Sakoda M, Tago K, Kamijo T, Ohta H, Nishizawa T. A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima. Microorganisms. 2023; 11(2):260. https://doi.org/10.3390/microorganisms11020260

Chicago/Turabian Style

Arsyadi, Ahmad, Yong Guo, Akiko Ebihara, Nobuo Sakagami, Midori Sakoda, Kanako Tago, Takashi Kamijo, Hiroyuki Ohta, and Tomoyasu Nishizawa. 2023. "A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima" Microorganisms 11, no. 2: 260. https://doi.org/10.3390/microorganisms11020260

APA Style

Arsyadi, A., Guo, Y., Ebihara, A., Sakagami, N., Sakoda, M., Tago, K., Kamijo, T., Ohta, H., & Nishizawa, T. (2023). A Nitrate-Transforming Bacterial Community Dominates in the Miscanthus Rhizosphere on Nitrogen-Deficient Volcanic Deposits of Miyake-jima. Microorganisms, 11(2), 260. https://doi.org/10.3390/microorganisms11020260

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