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Distinct contributions of suspended and sinking prokaryotes to mesopelagic carbon budget

Nature Geoscience (2026)Cite this article

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Abstract

The mesopelagic zone, between 100 m and 1,000 m depth, is a crucial layer in which carbon preliminary coming down from the surface is transformed before a portion makes it into the deep ocean. While eddies and their fronts influence surface productivity and carbon export, their effects deeper in the water column remain poorly understood. Here we show the importance and contribution of dark carbon fixation—the conversion of inorganic into organic carbon by prokaryotes—across five contrasting hydrological features in the North Atlantic, using isotopic tracers and quantification of chemoautotrophy genes. The approach allows simultaneous assessment of dark carbon fixation and heterotrophic activity of prokaryotes living suspended in seawater and attached to gravitationally settling particles. Our results highlight that heterotrophic prokaryotes attached to sinking particles contribute up to 21% of the total organic carbon required to sustain prokaryotic metabolism under the influence of eddy fronts. By contrast, dark carbon fixation by suspended prokaryotes can contribute up to half of the total carbon input to the mesopelagic zone in the cyclonic eddy. Our findings challenge the idea that carbon cycling in the mid-depth ocean is uniform and highlight the need to integrate microbial fractions and physical heterogeneity into ocean carbon models.

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Fig. 1: Overview of sampling sites.
Fig. 2: Depth profiles of prokaryotic activities.
Fig. 3: Chemolithoautotrophic fixation pathways.
Fig. 4: Single-cell substrate assimilation and metabolic classification by nanoSIMS at site PSS3, 500 m water depth.
Fig. 5: Mesopelagic carbon budgets of the five stations (PSSs) resulting from the APERO cruise.

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Data availability

All data generated and used in this study are available via SEANOE (Sea Scientific Open Data Edition) at https://doi.org/10.17882/103735. The dataset, titled ‘Biogeochemical datasets collected during the APERO cruise’, is structured by methodological approach and includes all biogeochemical, microbial and environmental measurements used in the present study. No external or publicly available datasets were used in this study.

Code availability

The code used for data processing and figure generation is not custom developed and consists only of standard scripts. It is available from the corresponding author upon request. No publicly archived version is provided.

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Acknowledgements

This Article contributes to the APERO project funded by the National Research Agency under the grant APERO (grant no. ANR ANR-21-CE01-0027) and by the French LEFE-Cyber programme (CNRS, INSU). The authors thank the captain and crew of N/O ‘Le Pourquoi Pas’ (Flotte Océanographique Française) for their help during the APERO cruise (https://doi.org/10.17600/1800066). We thank the ‘Moyen Commun’ SAM and Radioactivity from the Mediterranean Institute of Oceanography (MIO) as well as the ‘parc national d’instrumentation océanographique’ (PNIO) of the ‘division technique de l’Institut national des sciences de l’Univers du CNRS (DT INSU) for their technical expertise and facilities. This work was also supported by the Pure Ocean Fund via the Microcean project granted to P.L.C. and by ANR-JC ARMORIC-ANR-21-CE01-0005 granted to F.L.M. This work was funded by the European Union under grant agreement no. 101083922 (OceanICU) and UK Research. The views and opinions expressed are, however, those of the author(s) only and do not necessarily reflect those of the European Union or European Research Executive Agency. Neither the European Union nor the granting authority can be held responsible for them.

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Authors and Affiliations

  1. Aix Marseille Université, Université de Toulon, CNRS, IRD, Mediterranean Institute of Oceanography, Marseille, France

    Pauline Le Coq, France Van Wambeke, Elisabeth Chevillon, Bruno Zakardjian, Marc Garel, Sophie Guasco, Patricia Bonin, Badr Al Ali, Olivier Grosso, Thierry Moutin, Nagib Bhairy, Fabrice Armougom & Christian Tamburini

  2. Université Littoral Côte d’Opale, CNRS, Université de Lille, UMR 8187 LOG, Wimereux, France

    Urania Christaki

  3. Department of Earth System Science, Stanford University, Stanford, CA, USA

    Chloé M. J. Baumas & Anne E. Dekas

  4. Université Brest, CNRS, IRD, IFREMER, Laboratoire des Sciences de l’Environnement Marin, Plouzané, France

    Chloé M. J. Baumas, Maéva Gesson, Frédéric Le Moigne & Laurent Memery

  5. Sorbonne Université, CNRS, Laboratoire d’Océanographie Microbienne, LOMIC, Banyuls-sur-Mer, France

    Mireille Pujo-Pay & Olivier Crispi

  6. CNRS, Parc National d’Instrumentation Océanographique, Division Technique de l’INSU – UPS855, Plouzané, France

    Emmanuel de Saint Léger

  7. Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche, LOV, Villefranche-sur-Mer, France

    Lionel Guidi

  8. Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, Paris, France

    Lionel Guidi

  9. Department of Plankton and Microbial Ecology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, Stechlin, Germany

    Hans-Peter Grossart

  10. Institute of Biochemistry and Biology, Potsdam University, Potsdam, Germany

    Hans-Peter Grossart

Authors
  1. Pauline Le Coq
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  2. Urania Christaki
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  3. France Van Wambeke
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Contributions

P.L.C. and C.T. conceived this work; P.L.C., U.C., F.V.W., B.A.A., M. Garel, C.T., S.G., C.M.J.B., M.P.P., M. Gesson, F.L.M., E.C., T.M., O.C., N.B., E.d.S.L. and O.G. conducted fieldwork and/or laboratory analysis; C.T., U.C., F.V.W., H.-P.G., A.E.D., P.B., F.A., B.Z., L.G. and L.M. advised on interpretations. P.L.C. wrote the manuscript, with all authors contributing to its revision.

Corresponding authors

Correspondence to Pauline Le Coq or Christian Tamburini.

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Extended data

Extended Data Fig. 1 Hydrological conditions and surface Chlorophyll a during the APERO cruise.

(A) Conservative temperature (ϴ) and absolute salinity (SA) diagram of the five Process Studies Stations (PSS1 to PSS5 in yellow, light blue, green, brown and purple, respectively). NEACW: Northeast Atlantic Central Water; NEABW: Northeast Atlantic Bottom Water; MW: Mediterranean Water; SAIW: Subarctic Intermediate Water; LSW: Labrador Sea Water; Polar-like SW: Surface Water; (B) Time series of remote sensed Chlorophyll a (Chl.a) surface concentrations averaged over the area sampled by the PSS (squared area from minima/maxima of the drifting mooring line positions) from April 1 to August 31, 2023, and timings of the APERO cruise (thin black line) and PSSs (thick red line). Chl.a data are L3 (dark-green crosses) and L4 (green line) CMEMS North Atlantic 1 km resolution GlobColour products. Data from refs. 70,71.

Extended Data Fig. 2 Biogeochemical characteristics of the mesopelagic zone (100 - 1000 m depths).

Particulate organic carbon (POC), dissolved organic carbon (DOC), nitrates plus nitrites (NOx) and ammonium (NH4) concentrations sampled with Niskin bottles (panels A, C, D and E) and sinking POC fluxes measured by the sediment traps over 4 days (panel B). These measurements were done on the five Process Studies Stations (PSSs) during the APERO cruise.

Extended Data Fig. 3 Illustration of the sampling methods employed during the APERO cruise to study prokaryotic fraction.

“Suspended” prokaryotes (that is, free-living and attached to suspended particles) and “sinking” prokaryotes (that is, attached to sinking particles) were sampled by Niskin and sediment traps respectively. The investigation of prokaryotic communities included PHP (3H-leucine) and DCF (14C-bicarbonate) measurements, prokaryotic cell abundance and gene quantification (qPCR) of chemoautotrophy in all PSSs. A single cell nanoSIMS analysis (13C-bicarbonate and 15N-ammonium) was added in PSS3 at 500 m. CTD rosette illustration reproduced with permission from ref. 72.

Extended Data Fig. 4 Boxplots of prokaryotic activities in the mesopelagic zone.

Rates of dark carbon fixation (yellow) and prokaryotic heterotrophic production (blue) were measured at the five PSSs (expressed in µmol C m⁻³ d⁻¹). Upper panels represent the “suspended” fraction (free-living prokaryotes and those attached to suspended particles), whereas lower panels represent the “sinking” fraction (prokaryotes attached to sinking particles). Each boxplot integrates measurements at 100, 200, 500, and 1000 m, with each depth analyzed in triplicate technical incubations (n = 12 data points per PSS). Technical replicates correspond to independent incubations of subsamples from the same Niskin or sediment trap collection. Boxplots (A), (B), (D), and (E) compare activities between PSSs, while (C) and (F) compare activities between fractions. Boxplots indicate the interquartile range (boxes), median (central line), and whiskers extending to 1.5×IQR. Statistical differences were assessed using Kruskal-Wallis multiple tests followed by Dunn post-hoc tests (* = p < 0.05) and the Wilcoxon-Mann-Whitney test (**** = p < 0.0001). Upper and lower panels cannot be compared directly, as the sampled volumes differ between Niskin bottles and sediment traps.

Extended Data Fig. 5 Normalized prokaryotic activity rates.

Rates normalized by (A) the prokaryotic cell abundance and (B) the organic carbon content. Each boxplot includes data pooled from all sampled stations and depths (n = 20). Overlayed boxplots indicate the interquartile range (boxes), median (central line), and whiskers extending to 1.5×IQR. Statistically significant differences are indicated with asterisks (two-sided Wilcoxon-Mann-Whitney statistical: **** p ≤ 0.0001; ** p < 0.01; * p < 0.05; Non-significative-NS).

Extended Data Fig. 6 Chemolithoautotrophic gene quantification.

Each boxplot includes data pooled from all sampled stations and depths (n = 20). Overlayed boxplots indicate the interquartile range (boxes), median (central line), and whiskers extending to 1.5×IQR. Statistically significant differences are indicated with asterisks (two-sided Wilcoxon-Mann-Whitney statistical test: **** p ≤ 0.0001; *** p < 0.001; * p < 0.05). (A) Ratio of total chemolithoautotrophic communities (gene copy numbers calculated as the sum of the marker genes accA, cbbL and cbbM) in the entire prokaryotic community (sum of bacterial and archaeal 16S gene copy numbers). qPCR gene ratio for AOA (ratio of amoA gene / 16S prokaryotes gene) and AOB (ratio of amoB gene / 16S prokaryotes gene) in (B) the “Suspended” fraction (that is, free-living and prokaryotes attached to suspended particles) and in (C) the “Sinking” fraction (that is, prokaryotes attached to sinking particles).

Extended Data Fig. 7 Chemolithoautotrophic fixation pathways.

Boxplot of qPCR gene ratio of the “suspended” fraction (that is, free-living and prokaryotes attached to suspended particles) and the “sinking” fraction (that is, prokaryotes attached to sinking particles). Each data point represents a ratio measured in the five PSSs at depths of 100, 200, 500, and 1000 m. Overlayed boxplots indicate the interquartile range (boxes), median (central line), and whiskers extending to 1.5×IQR. Statistically significant differences are indicated with asterisks (two-sided Wilcoxon-Mann-Whitney statistical test, **** p ≤ 0.0001; *** p < 0.001; ** p < 0.01). (A) Ratio of accA gene / 16S prokaryotes gene, proxy of chemolithoautotrophic prokaryotes using the 3-hydroxypropionate/4-hydroxybutyrate (3-HP/4-HB) pathway. (B) Ratio of cbbL gene / 16S prokaryotes gene, proxy of chemoautotrophic prokaryotes using Form I Rubisco of the Calvin-Benson-Bassham (CBB) cycle. (C) Ratio of cbbM gene / 16S prokaryotes gene, proxy of chemolithoautotrophic prokaryotes using Form II Rubisco of the CBB cycle. (D) Ratio of amoA (AOA + AOB) genes / 16S prokaryotes gene, proxy of ammonia oxidizers. (E) Ratio of total chemolithoautotrophic communities (gene copy numbers calculated as the sum of the marker genes accA, cbbL and cbbM) in the entire prokaryotic community (sum of bacterial and archaeal 16S gene copy numbers).

Extended Data Fig. 8 Mesopelagic carbon budgets of the five stations (PSSs) resulting from the APERO cruise.

The input of carbon to the mesopelagic (ΔPOC plus dark carbon fixation fluxes) were compared to the prokaryotic carbon demand integrated between depths of 100 and 1000 m depths, expressed in mg C m−2 d−1. The legend is detailed above, with the “suspended” fraction that includes free-living and prokaryotes attached to suspended particles, and the “sinking” fraction that corresponds to prokaryotes attached to sinking particles. We applied a PGEsinking of 0.24 and PGESuspended of 0.08 as in29. At PSS2 the lack of DCFSuspended values prevented integration. DCFsinking is <1% and therefore not visible.

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Le Coq, P., Christaki, U., Van Wambeke, F. et al. Distinct contributions of suspended and sinking prokaryotes to mesopelagic carbon budget. Nat. Geosci. (2026). https://doi.org/10.1038/s41561-025-01888-w

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