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Evidence of the Significant Contribution of Heterotrophic Diazotrophs to Nitrogen Fixation in the Eastern Indian Ocean During Pre-Southwest Monsoon Period

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Abstract

Nitrogen fixation continually transforms atmospheric nitrogen (N2) into biologically available nitrogen in the oceans, which actively sustains marine new production, especially in oligotrophic ecosystems. Recently, heterotrophic diazotrophs were found to be widespread and potentially important for nitrogen fixation in the Eastern Indian Ocean (EIO). However, no direct measurement has been taken in this region to explore the contribution of heterotrophic diazotrophs to total nitrogen fixation. To address this gap, we examined size-fractioned nitrogen fixation rates (NFRs) using an isotope 15 N tracer technique, diazotroph community structure analysis based on molecular detection, and primary productivity (PP) measurements using an isotope 14C tracer technique within the euphotic zone of the EIO during the pre-southwest monsoon period. Our results reveal that diazotroph communities are dominated by heterotrophic diazotrophs and filamentous cyanobacteria in the surface waters of the EIO. Size-fractioned data show that the < 10 μm fraction of the NFRs is major contributors to the total NFRs throughout the water column. Notably, the isotopically derived NFRs show that the > 10 μm fraction exhibits spatial heterogeneity in the surface samples, with significantly higher rates in the Bay of Bengal (BoB) compared to the southeastern Indian Ocean. Correspondingly, the NFRs of the > 10 μm fraction match well with high-throughput sequencing and microscope counts. In comparison, the NFRs of the < 10 μm fraction do not display significant regional differences, which is attributed to the major fixation efficiency by different bacteria. Based on the Redfield ratio (C:N = 6.6:1), depth-integrated NFRs were estimated to contribute 0.3–1.3% of the total PP in the study region. Overall, our study provides baseline NFRs in the EIO and highlights the potential importance of non-cyanobacteria to nitrogen fixation. Our findings have significance in the biogeochemical understanding of the coupling between nitrogen and carbon cycling in the oligotrophic Indian Ocean.

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Data Availability

Data and computer codes for analyses are available in GitHub repository: https://github.com/phytoplankton-sunjun/Wu-chao-Ecosystems-2021-main.git

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Acknowledgements

We thank Prof. Dongxiao Wang from South China Sea Institute of Oceanology, Chinese Academy of Sciences for providing hydrographic (CTD) data. Dr. Liangliang Kong at South China Sea Institute of Oceanology of Chinese Academy of Sciences and Dr. Misun Yun at Tianjin University of Science and Technology are also acknowledged for their help and technical support during experiments. We would also like to thank the Open Cruise Project in Eastern Indian Ocean of National Nature Science Foundation of China (NORC2018-10) for sharing their ship time and gratefully acknowledge the crew of R/V “Shiyan 3” and all participants for their assistance during the cruise.

Funding

This work was supported by the National Natural Science Foundation of China (41876134, 41676112, 41706184, 41276124, and 42106095), the Tianjin 131 Innovation Team Program (20180314), and the Changjiang Scholar Program of Chinese Ministry of Education (T2014253) to Jun Sun.

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  1. Research Centre for Indian Ocean Ecosystem, Tianjin University of Science and Technology, Tianjin, 300457, China

    Chao Wu, Jun Sun, Haijiao Liu, Wenzhe Xu, Guicheng Zhang & Yiyan Guo

  2. College of Marine Science and Technology, China University of Geosciences (Wuhan), Wuhan, 430074, Hubei, China

    Jun Sun

  3. College of Environmental Science and Engineering, Ocean University of China, Qingdao, 266100, China

    Hanfang Lu

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  1. Chao Wu
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JS conceived and designed the study. CW, HJL, WZX, GCZ, and YYG performed the research. CW wrote the paper. JS, HJL, WZX, GCZ, HFL, and YYG edited the paper.

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Correspondence to Jun Sun.

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Wu, C., Sun, J., Liu, H. et al. Evidence of the Significant Contribution of Heterotrophic Diazotrophs to Nitrogen Fixation in the Eastern Indian Ocean During Pre-Southwest Monsoon Period. Ecosystems 25, 1066–1083 (2022). https://doi.org/10.1007/s10021-021-00702-z

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