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Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean

A Correction to this article was published on 20 January 2022

This article has been updated

Abstract

Biological nitrogen fixation contributes significantly to marine primary productivity. The current view depicts few cyanobacterial diazotrophs as the main marine nitrogen fixers. Here, we used 891 Tara Oceans metagenomes derived from surface waters of five oceans and two seas to generate a manually curated genomic database corresponding to free-living, filamentous, colony-forming, particle-attached, and symbiotic bacterial and archaeal populations. The database provides the genomic content of eight cyanobacterial diazotrophs including a newly discovered population related to known heterocystous symbionts of diatoms, as well as 40 heterotrophic bacterial diazotrophs that considerably expand the known diversity of abundant marine nitrogen fixers. These 48 populations encapsulate 92% of metagenomic signal for known nifH genes in the sunlit ocean, suggesting that the genomic characterization of the most abundant marine diazotrophs may be nearing completion. Newly identified heterotrophic bacterial diazotrophs are widespread, express their nifH genes in situ, and also occur in large planktonic size fractions where they might form aggregates that provide the low-oxygen microenvironments required for nitrogen fixation. Critically, we found heterotrophic bacterial diazotrophs to be more abundant than cyanobacterial diazotrophs in most metagenomes from the open oceans and seas, emphasizing the importance of a wide range of heterotrophic populations in the marine nitrogen balance.

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Fig. 1: The phylogeny of 48 marine bacterial diazotrophs.
Fig. 2: Functional lifestyle of marine diazotrophs.
Fig. 3: Oceanic stations with highest metagenomic signal for diazotrophs.
Fig. 4: Detection of nifH genes across marine metagenomes and metatranscriptomes.

Data availability

All data our study generated are publicly available at http://www.genoscope.cns.fr/tara/ (metagenomic co-assemblies, FASTA files) or https://figshare.com/articles/dataset/Marine_diazotrophs/14248283 for the supplemental tables and information, as well as the genomic content of 48 marine diazotrophs using the new nomenclature (diazotrophic genomic database).

Change history

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Acknowledgements

Our survey was made possible by two scientific endeavors: the sampling and sequencing efforts by the Tara Oceans Project, and the bioinformatics and visualization capabilities afforded by anvi’o. We are indebted to all who contributed to these efforts, as well as other open-source bioinformatics tools for their commitment to transparency and openness. Tara Oceans (which includes the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Oceans Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org/). Some of the computations were performed using the platine, titane and curie HPC machine provided through GENCI grants (t2011076389, t2012076389, t2013036389, t2014036389, t2015036389, and t2016036389). This work has been supported by the FFEM - French Facility for Global Environment, French Government ‘Investissements d’Avenir’ programs OCEANOMICS (ANR-11-BTBR- 0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX- 54), and PSL Research University (ANR-11-IDEX-0001-02). C.B. additionally acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (Diatomic; grant agreement No. 835067) and Agence Nationale de la Recherche “Phytomet” (ANR-16-CE01-0008) projects. Finally, RAF is supported by the Knut and Alice Wallenberg Foundation. JJPK acknowledges postdoctoral funding from the Fonds Français pour l’Environnement Mondial and Iva Veseli acknowledges support by the National Science Foundation Graduate Research Fellowship under Grant No. 1746045.

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Contributions

T. O. Delmont conducted the study and performed the primary data analysis. Eric Pelletier and Juan Pierella Karlusich performed analyses regarding the abundance of MAGs and nifH genes (including helping creating the extended nifH gene database) across Tara Oceans metagenomes and metatranscriptomes. Iva Veseli and Jessika Fuessel performed functional analyses of the diazotrophic MAGs. A. M. Eren computed to compatibility between nifH genes and widely used primers. All authors helped interpret the data. T. O. Delmont wrote the manuscript, with critical inputs from all the authors.

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Correspondence to Tom O. Delmont.

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The original online version of this article was revised:

In this article the References 30 – 32 were not given in the correct order in List of References: The correct order is given below

30. Benavides M, Moisander PH, Daley MC, Bode A, Arístegui J (2016). Longitudinal variability of diazotroph abundances in the subtropical North Atlantic Ocean. J Plankton Res. https://doi.org/10.1093/plankt/fbv121.

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32. Man-Aharonovich D, Kress N, Zeev EB, Berman-Frank I, Béjà O. Molecular ecologyof nifH genes and transcripts in the eastern Mediterranean Sea. Environ Microbiol.2007;9:2354–63.

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Delmont, T.O., Pierella Karlusich, J.J., Veseli, I. et al. Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean. ISME J 16, 927–936 (2022). https://doi.org/10.1038/s41396-021-01135-1

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