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Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods

J J Pierella Karlusich, E Pelletier, F Lombard [...] E Karsenti, C de Vargas, P Wincker, C Bowler & R A. Foster

Juan José Pierella Karlusich, Eric Pelletier, Fabien Lombard, Madeline Carsique, Etienne Dvorak, Sébastien Colin, Marc Picheral, Francisco M. Cornejo-Castillo, Silvia G. Acinas, Rainer Pepperkok, Eric Karsenti, Colomban de Vargas, Patrick Wincker, Chris Bowler & Rachel A. Foster

Abstract

Nitrogen fixation has a critical role in marine primary production, yet our understanding of marine nitrogen-fixers (diazotrophs) is hindered by limited observations. Here, we report a quantitative image analysis pipeline combined with mapping of molecular markers for mining >2,000,000 images and >1300 metagenomes from surface, deep chlorophyll maximum and mesopelagic seawater samples across 6 size fractions (<0.2–2000 μm). We use this approach to characterise the diversity, abundance, biovolume and distribution of symbiotic, colony-forming and particle-associated diazotrophs at a global scale. We show that imaging and PCR-free molecular data are congruent. Sequence reads indicate diazotrophs are detected from the ultrasmall bacterioplankton (<0.2 μm) to mesoplankton (180–2000 μm) communities, while images predict numerous symbiotic and colony-forming diazotrophs (>20 µm). Using imaging and molecular data, we estimate that polyploidy can substantially affect gene abundances of symbiotic versus colony-forming diazotrophs. Our results support the canonical view that larger diazotrophs (>10 μm) dominate the tropical belts, while unicellular cyanobacterial and non-cyanobacterial diazotrophs are globally distributed in surface and mesopelagic layers. We describe co-occurring diazotrophic lineages of different lifestyles and identify high-density regions of diazotrophs in the global ocean. Overall, we provide an update of marine diazotroph biogeographical diversity and present a new bioimaging-bioinformatic workflow.

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Nat Commun. 12, Art. : 4160 (2021) doi : 10.1038/s41467-021-24299-y