Sinking Trichodesmium fixes nitrogen in the dark ocean

Mar Benavides, Sophie Bonnet, Frédéric A.C. Le Moigne, Gabrielle Armin, Keisuke Inomura, Søren Hallstrøm, Lasse Riemann, Ilana Berman-Frank, Emilie Poletti, Marc Garel, Olivier Grosso, Karine Leblanc, Catherine Guigue, Marc Tedetti, Cécile Dupouy

Research output: Contribution to journalArticlepeer-review

Abstract

The photosynthetic cyanobacterium Trichodesmium is widely distributed in the surface low latitude ocean where it contributes significantly to N2 fixation and primary productivity. Previous studies found nifH genes and intact Trichodesmium colonies in the sunlight-deprived meso- and bathypelagic layers of the ocean (200–4000 m depth). Yet, the ability of Trichodesmium to fix N2 in the dark ocean has not been explored. We performed 15N2 incubations in sediment traps at 170, 270 and 1000 m at two locations in the South Pacific. Sinking Trichodesmium colonies fixed N2 at similar rates than previously observed in the surface ocean (36–214 fmol N cell−1 d−1). This activity accounted for 40 ± 28% of the bulk N2 fixation rates measured in the traps, indicating that other diazotrophs were also active in the mesopelagic zone. Accordingly, cDNA nifH amplicon sequencing revealed that while Trichodesmium accounted for most of the expressed nifH genes in the traps, other diazotrophs such as Chlorobium and Deltaproteobacteria were also active. Laboratory experiments simulating mesopelagic conditions confirmed that increasing hydrostatic pressure and decreasing temperature reduced but did not completely inhibit N2 fixation in Trichodesmium. Finally, using a cell metabolism model we predict that Trichodesmium uses photosynthesis-derived stored carbon to sustain N2 fixation while sinking into the mesopelagic. We conclude that sinking Trichodesmium provides ammonium, dissolved organic matter and biomass to mesopelagic prokaryotes.

Original languageEnglish
JournalISME Journal
DOIs
StateAccepted/In press - 2022

Bibliographical note

Funding Information:
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 DOI: 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 and the Institut de Recherche pour le Développement (IRD). This research also received funding from INSU-LEFE grant DEFINE (MB), National Science Foundation EPSCoR Cooperative Agreement OIA-1655221 E (KI) and Danish Council for independent research 6108-00013 (SH and LR). The authors would like to thank the crew and technical staff of R/V L’Atalante as well as the scientists that participated in trap deployment onboard, as well as N. Brouilly and F. Richard at the IBDML SEM facility (Marseille, France). We are indebted to A. Vogts for nanoSIMS analyses (IOW, Warnemünde, Germany) and A. Filella (MIO, Marseille, France) for salinity effect experiments on Trichodesmium cultures. The authors are grateful to M. Sebastián, J.M. Gasol, J. Arístegui and X.A. Álvarez-Salgado for their comments on previous versions of this manuscript.

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to International Society for Microbial Ecology.

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

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