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Sinking Trichodesmium fixes nitrogen in the dark ocean

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.

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Fig. 1: Trichodesmium-specific 15N atom % enrichment.
Fig. 2: Diazotroph community expression profiles.
Fig. 3: Trichodesmium culture sinking simulation experiments.
Fig. 4: Relationship between the initial carbon storage to biomass ratio (initial RSto) of Trichodesmium cells and the depth at which cell carbon storage is depleted.

Data availability

All data are available in the main text or the supplementary materials. The model code for this study can be found in https://zenodo.org/record/5153594 (DOI: 10.5281/zenodo.5153594). Sequences have been deposited in the Sequence Read Archive under accession number PRJNA742179.

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Acknowledgements

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.

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MB conceptualized the research and carried out formal analysis of the data; MB and SB performed field experiments assisted by IBF and CG; FACLM designed sediment trap deployments and performed sinking velocity calculations; GA and KI developed the cell metabolism model; SH performed bioinformatics analyses; EP and MG performed sinking simulation lab experiments; OG analyzed EA-IRMS and MIMS samples; KL performed lithogenic silica analyses; CG performed CDOM/FDOM field sampling; MT analyzed CDOM/FDOM data; CD measured CDOM/FDOM from cultures; MB wrote the manuscript with input from SB, FACLM, KI, LR and IBF.

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Correspondence to Mar Benavides.

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Benavides, M., Bonnet, S., Le Moigne, F.A.C. et al. Sinking Trichodesmium fixes nitrogen in the dark ocean. ISME J 16, 2398–2405 (2022). https://doi.org/10.1038/s41396-022-01289-6

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