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Microbial Ecology

, Volume 78, Issue 4, pp 804–819 | Cite as

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

  • Chao Wu
  • Jinjun Kan
  • Haijiao Liu
  • Laxman Pujari
  • Congcong Guo
  • Xingzhou Wang
  • Jun SunEmail author
Microbiology of Aquatic Systems

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.

Keywords

Diazotroph Heterotrophic bacteria Trichodesmium High throughput sequencing Nitrogen fixation The eastern Indian Ocean 

Notes

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.

Author 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.

Funding Information

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.

Supplementary material

248_2019_1355_Fig9_ESM.png (5.2 mb)
Fig. S1

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

248_2019_1355_MOESM1_ESM.tif (1.5 mb)
High resolution image (TIF 1530 kb)
248_2019_1355_Fig10_ESM.png (1.2 mb)
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)

248_2019_1355_MOESM2_ESM.tif (2.6 mb)
High resolution image (TIF 2708 kb)
248_2019_1355_MOESM3_ESM.docx (23 kb)
Supplementary Table 1 (DOCX 22 kb)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Marine Science and TechnologyShandong UniversityQingdaoChina
  2. 2.Microbiology DivisionStroud Water Research CenterAvondaleUSA
  3. 3.Tianjin Key Laboratory of Marine Resources and ChemistryTianjin University of Science and TechnologyTianjinChina
  4. 4.Research Centre for Indian Ocean EcosystemTianjin University of science and TechnologyTianjinChina
  5. 5.College of Marine & Environmental SciencesTianjin University of Science and TechnologyTianjinPeople’s Republic of China

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