Diazotrophs are overlooked contributors to carbon and nitrogen export to the deep ocean

Sophie Bonnet, Mar Benavides, Frédéric A.C. Le Moigne, Mercedes Camps, Antoine Torremocha, Olivier Grosso, Céline Dimier, Dina Spungin, Ilana Berman-Frank, Laurence Garczarek, Francisco M. Cornejo-Castillo

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

Diazotrophs are widespread microorganisms that alleviate nitrogen limitation in 60% of our oceans, thereby regulating marine productivity. Yet, the group-specific contribution of diazotrophs to organic matter export has not been quantified, which so far has impeded an accurate assessment of their impact on the biological carbon pump. Here, we examine the fate of five groups of globally-distributed diazotrophs by using an original combination of mesopelagic particle sampling devices across the subtropical South Pacific Ocean. We demonstrate that cyanobacterial and non-cyanobacterial diazotrophs are exported down to 1000 m depth. Surprisingly, group-specific export turnover rates point to a more efficient export of small unicellular cyanobacterial diazotrophs (UCYN) relative to the larger and filamentous Trichodesmium. Phycoerythrin-containing UCYN-B and UCYN-C-like cells were recurrently found embedded in large (>50 µm) organic aggregates or organized into clusters of tens to hundreds of cells linked by an extracellular matrix, presumably facilitating their export. Beyond the South Pacific, our data are supported by analysis of the Tara Oceans metagenomes collected in other ocean basins, extending the scope of our results globally. We show that, when diazotrophs are found in the euphotic zone, they are also systematically present in mesopelagic waters, suggesting their transport to the deep ocean. We thus conclude that diazotrophs are a significant part of the carbon sequestered in the deep ocean and, therefore, they need to be accounted in regional and global estimates of export.

Original languageEnglish
Pages (from-to)47-58
Number of pages12
JournalISME Journal
Volume17
Issue number1
DOIs
StatePublished - Jan 2023
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2022, The Author(s).

Funding

This research is a contribution of the TONGA project (Shallow hydroThermal sOurces of trace elemeNts: potential impacts on biological productivity and the bioloGicAl carbon pump; TONGA cruise https://doi.org/10.17600/18000884 ) funded by the Agence Nationale de la Recherche (grant TONGA ANR-18- CE01-0016 and grant CINNAMON ANR-17-CE2-0014-01), the LEFE-CyBER program (CNRS-INSU), the A-Midex foundation, the Institut de Recherche pour le Développement (IRD). FMCC and LG acknowledge funding from the European Union’s Horizon 2020 research programme under the Marie Sklodowska-Curie grant agreement No. 749380 (UCYN2PLAST). FMCC has also received the support of a fellowship (grant no. 105090) from”la Caixa” Foundation (ID 100010434) and from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 847648”, and acknowledges funding from the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S). The authors warmly thank the crew of the R/V L’Atalante for outstanding shipboard operations. Nagib Bhairy is warmly thanked for his efficient help with MSC deployment and clean CTD rosette management, Vincent Taillandier for CTD data processing, Sandra Nunige for nutrient analyses, and Karine Leblanc for Phenom images acquisition.

FundersFunder number
A-Midex foundation
Spanish GovernmentCEX2019-000928-S
Horizon 2020 Framework Programme
H2020 Marie Skłodowska-Curie ActionsUCYN2PLAST, 100010434, 847648, 105090, 749380
Institut de recherche pour le développement
Agence Nationale de la RechercheCINNAMON ANR-17-CE2-0014-01, TONGA ANR-18- CE01-0016
Institut national des sciences de l'Univers

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