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

Tom O. Delmont, Juan José Pierella Karlusich, Iva Veseli, Jessika Fuessel, A. Murat Eren, Rachel A. Foster, Chris Bowler, Patrick Wincker, Eric Pelletier
doi: https://doi.org/10.1101/2021.03.24.436778
Tom O. Delmont
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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  • For correspondence: tomodelmont@gmail.com
Juan José Pierella Karlusich
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
3Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
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Iva Veseli
4Graduate Program in Biophysical Sciences, University of Chicago, Chicago, Illinois 60637, USA
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Jessika Fuessel
5Department of Medicine, University of Chicago, Chicago, Illinois 60637, USA
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A. Murat Eren
5Department of Medicine, University of Chicago, Chicago, Illinois 60637, USA
6Bay Paul Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA
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Rachel A. Foster
7Department of Ecology, Environment and Plant Sciences, Stockholm University Stockholm, 106 91, Sweden
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Chris Bowler
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
3Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
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Patrick Wincker
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Eric Pelletier
1Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
2Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOsee, Paris, France
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Abstract

Biological nitrogen fixation is a major factor contributing to microbial primary productivity in the open ocean. The current view depicts a few cyanobacterial diazotrophs as the most relevant marine nitrogen fixers, whereas heterotrophic diazotrophs are more diverse and considered to have lower impacts on the nitrogen balance. Here, we used 891 Tara Oceans metagenomes to create a manually curated, non-redundant genomic database corresponding to free-living, as well as filamentous, colony-forming, particle-attached and symbiotic bacterial and archaeal populations occurring in the surface of five oceans and two seas. Notably, the database provided the genomic content of eight cyanobacterial diazotrophs including Trichodesmium populations and a newly discovered population similar to Richelia, as well as 40 heterotrophic bacterial diazotrophs organized into three main functional groups that considerably expand the known diversity of abundant marine nitrogen fixers compared to previous genomic surveys. Critically, these 48 populations may account for more than 90% of cells containing known nifH genes and occurring in the sunlit ocean, suggesting that the genomic characterization of the most abundant marine diazotrophs may be nearing completion. The newly identified heterotrophic bacterial diazotrophs are widespread, express their nifH genes in situ, and co-occur under nitrate-depleted conditions in large size fractions where they might form aggregates providing the low-oxygen microenvironments required for nitrogen fixation. Most significantly, we found heterotrophic bacterial diazotrophs to be more abundant than cyanobacterial diazotrophs in most metagenomes from the open oceans and seas. This large-scale environmental genomic survey emphasizes the considerable potential of heterotrophs in the marine nitrogen balance.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.genoscope.cns.fr/tara/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean
Tom O. Delmont, Juan José Pierella Karlusich, Iva Veseli, Jessika Fuessel, A. Murat Eren, Rachel A. Foster, Chris Bowler, Patrick Wincker, Eric Pelletier
bioRxiv 2021.03.24.436778; doi: https://doi.org/10.1101/2021.03.24.436778
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Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean
Tom O. Delmont, Juan José Pierella Karlusich, Iva Veseli, Jessika Fuessel, A. Murat Eren, Rachel A. Foster, Chris Bowler, Patrick Wincker, Eric Pelletier
bioRxiv 2021.03.24.436778; doi: https://doi.org/10.1101/2021.03.24.436778

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