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Heterotrophic Bacteria Dominate the Diazotrophic Community in the Eastern Indian Ocean (EIO) during Pre-Southwest Monsoon

  • Microbiology of Aquatic Systems
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Abstract

The diazotrophic communities play an important role in sustaining primary productivity through adding new nitrogen to oligotrophic marine ecosystems. Yet, their composition in the oligotrophic Indian Ocean is poorly understood. Here, we report the first observation of phylogenetic diversity and distribution of diazotrophs in the Eastern Indian Ocean (EIO) surface water (to 200 m) during the pre-southwest monsoon period. Through high throughput sequencing of nifH genes, we identified diverse groups of diazotrophs in the EIO including both non-cyanobacterial and cyanobacterial phylotypes. Proteobacteria (mainly Alpha-, Beta-, and Gamma-proteobacteria) were the most diverse and abundant groups within all the diazotrophs, which accounted for more than 86.9% of the total sequences. Cyanobacteria were also retrieved, and they were dominated by the filamentous non-heterocystous cyanobacteria Trichodesmium spp. Other cyanobacteria such as unicellular diazotrophic cyanobacteria were detected sporadically. Interestingly, our qPCR analysis demonstrated that the depth-integrated gene abundances of the diazotrophic communities exhibited spatial heterogeneity with Trichodesmium spp. appeared to be more abundant in the Bay of Bengal (p < 0.05), while Sagittula castanea (Alphaproteobacteria) was found to be more dominating in the equatorial region and offshores (p < 0.05). Non-metric multidimensional scaling analysis (NMDS) further confirmed distinct vertical and horizontal spatial variations in the EIO. Canonical correspondence analysis (CCA) indicated that temperature, salinity, and phosphate were the major environmental factors driving the distribution of the diazotroph communities. Overall, our study provides the first insight into the diversity and distribution of the diazotrophic communities in EIO. The findings from this study highlight distinct contributions of both non-cyanobacteria and cyanobacteria to N2 fixation. Moreover, our study reveals information that is critical for understanding spatial heterogeneity and distribution of diazotrophs, and their vital roles in nitrogen and carbon cycling.

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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 McGill University and Dr. Xiaomin Xia at the Hong Kong University of Science and Technology are also acknowledged for their help and technical support during experiments. We also gratefully acknowledge the crew of R/V “Shiyan 3” and all participants for their assistance during the cruise.

Funding

This study was supported by the National Natural Science Foundation of China (41876134, 41276124, and 41676112) and NSFC open research cruises (NORC2017-10), the Science Fund for University Creative Research Groups in Tianjin (TD12-5003), the Changjiang Scholar Program of Chinese Ministry of Education to JS, and endowment support from Stroud Water Research Center to JK.

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Authors and Affiliations

  1. Institute of Marine Science and Technology, Shandong University, Qingdao, 266237, China

    Chao Wu & Haijiao Liu

  2. Microbiology Division, Stroud Water Research Center, Avondale, PA, 19311, USA

    Jinjun Kan

  3. Tianjin Key Laboratory of Marine Resources and Chemistry, Tianjin University of Science and Technology, Tianjin, 300457, China

    Laxman Pujari, Congcong Guo, Xingzhou Wang & Jun Sun

  4. Research Centre for Indian Ocean Ecosystem, Tianjin University of science and Technology, Tianjin, 300457, China

    Laxman Pujari, Congcong Guo, Xingzhou Wang & Jun Sun

  5. College of Marine & Environmental Sciences, Tianjin University of Science and Technology, No.29 13th Avenue, TEDA, Tianjin, 300457, People’s Republic of China

    Jun Sun

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  1. Chao Wu
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  5. Congcong Guo
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  6. Xingzhou Wang
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  7. Jun Sun
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Contributions

This work was designed by JS. Samples were collected by CW, HL, and XW. CW performed experiments and analyzed data. CG performed the nutrients analysis. CW drafted the paper and revised by JK and PL. All authors contributed to the writing of the manuscript.

Corresponding author

Correspondence to Jun Sun.

Electronic Supplementary Material

Fig. S1

Depth profiles of dissolved inorganic nutrients (nitrate, nitrite, ammonium, phosphate, silicate) and Chl a in the EIO (PNG 5281 kb)

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(TIF 1530 kb)

Fig. S2

Rarefaction curves comparing the number of reads with the number of phylotypes (OTUs) found in the DNA libraries in the EIO. The last digit represented water depth: 1, 2 and 3 represent 0m, 75m and 200m, respectively. (PNG 1240 kb)

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(TIF 2708 kb)

Supplementary Table 1

(DOCX 22 kb)

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Wu, C., Kan, J., Liu, H. et al. Heterotrophic Bacteria Dominate the Diazotrophic Community in the Eastern Indian Ocean (EIO) during Pre-Southwest Monsoon. Microb Ecol 78, 804–819 (2019). https://doi.org/10.1007/s00248-019-01355-1

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  • DOI: https://doi.org/10.1007/s00248-019-01355-1

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