Abstract Bacteria are important agents modulating the efficiency of the ocean's biological carbon pump (BCP). The long‐standing view considers bacteria as degraders of sinking particulate organic carbon (POC), yet underappreciates their contribution to carbon export. Here, using in situ pump sampling, particle imaging, and bacterial biomarker analysis across the equatorial Pacific, we show that bacteria primarily accompany carbon flux passively, rather than actively attenuating it. Despite rapid attenuation of POC flux with depth in large sinking particles, chemical signatures suggest minimal bacterial remineralization. Nevertheless, bacterial material constituted ∼30% of the POC flux. Bacterial‐mediated POC attenuation was only ∼35% of the bacterial POC export. Such a pattern can be explained by rapid particle sinking and steep vertical temperature gradients, which limit bacterial metabolism but facilitate bacterial biomass export. Our findings reveal that bacteria serve as passive passengers in the BCP, largely contributing to rather than attenuating carbon flux.

Recent studies have shown that diazotrophs can form aggregates sinking at velocities up to 400 m d-1, challenging the long-standing assumption that these organisms are confined to the surface ocean, and suggesting an understimated role in carbon (C) sequestration in warm oligotrophic waters. Yet, the extent to which their biomass escapes remineralization in the mesopelagic zone remains poorly constrained. Here, we experimentally simulated the aggregation and sinking of the filamentous diazotroph Trichodesmium erythraeum using roller tanks, following organic matter distribution over a 10-day period-equivalent to a 1000 m descent at a sinking velocity of ~100 m d-1. Our results show that 33% of organic C and 36% of N remained in the particulate fraction at the end of the experiment, indicating that microbial remineralization was incomplete and relatively proportional. Remineralization was most intense during the first 3 to 5 days of descent (0-500 m), after which potential C flux declined. We also estimated that a substantial portion of bacterial biomass was incorporated into the aggregates and may contribute to the C export, revealing a dual role for bacteria as both recyclers and exporters of organic matter. Given the widespread distribution and high productivity of Trichodesmium erythraeum in the expanding (sub)tropical ocean, our results highlight the need to include its fate in global biogeochemical models.

The biological carbon pump contributes to set the magnitude of carbon sequestration in the oceans' interior. Estimating the relative contribution of microbial versus zooplankton‐mediated processes to particulate organic carbon (POC) flux attenuation provides insights into how this pump functions. Our study took place during the high productivity summer period in the Subantarctic and Polar Front Zone. In the upper mesopelagic (i.e., 180–300 m depth), we concurrently measured the downward POC flux, particle size and morphology, microbial remineralization rates and estimated size‐specific sinking velocities. These concomitant measurements revealed two different export systems, dominated by fecal material in the Subantarctic, and phyto‐aggregates in polar waters. These two systems were characterized by similar low particle sinking velocities (∼10 m d −1 ), while microbial remineralization rates differed by an order of magnitude. Higher microbial remineralization rates in the Subantarctic (0.11 d −1 ), compared to polar waters (0.04 d −1 ), were likely driven by the confounding effect of temperature and particle characteristics. Despite this difference in microbial remineralization rates, these two export systems were characterized by relatively similar transfer efficiencies, suggesting that microbes had differing influences. A comparison of microbially mediated (i.e., scaled using observed remineralization rates) with total POC flux attenuation (i.e., driven by the dual impact of microbes and flux‐feeders) revealed a higher microbial contribution to the flux attenuation in the upper mesopelagic of the subantarctic compared to the polar region. This deconstruction of the flux attenuation revealed an increasing influence of microbes on POC degradation with depth to become the predominant actor in the lower mesopelagic.

The ocean contributes to regulating atmospheric CO 2 levels via the biological carbon pump (BCP). One critical aspect of the BCP is the depth at which sinking particulate organic carbon (POC) remineralizes in the mesopelagic zone (200–1,000 m). In the Southern Ocean, the circulation is such that the products generated from POC remineralization may have drastically different fates depending on (a) the latitude at which sinking particulate material is produced and (b) the depth at which its remineralization occurs. Here, we assess latitudinal and depth variations of POC export marine aggregate abundance and composition in the Southeast Pacific sector of the Southern Ocean. We show changes in flux attenuation depth horizons in the upper mesopelagic in the subantarctic zone. These correspond to rapid particle accumulation below the depth of the euphotic zone followed by abrupt export. We believe that such rapid changes may be linked to diatom life cycles, including resting cell and spore formation and resulting changes in particle sinking velocities rather than attenuation due to heterotrophic degradation or solubilization in the upper mesopelagic zone. We further discuss the occurrence of such features in the Southern Ocean and at the global scale. Our results highlight the importance of alternative flux attenuation processes, such as sudden changes in particles sinking velocities, in explaining variability in organic carbon sequestration by the ocean's BCP.

Diatoms, a ubiquitous group of phytoplankton, account for approximately 40% of particulate organic carbon (POC) exported via the ocean biological carbon pump, which modulates atmospheric CO2. Diatoms are represented in global biogeochemical models as effective vectors for sinking POC, with their large size and dense skeletons made of biogenic Silica (BSi) thought to allow rapid transfer of organic carbon to the ocean interior. However, we observe this not to be the case across large parts of the Southern Ocean mesopelagic zone. Here we present direct flux measurements from different sectors of the Southern Ocean demonstrating that silica and carbon cycles in the Southern Ocean mesopelagic are strongly decoupled, with a weak mechanistic link between BSi and POC fluxes. By combining Marine Snow Catcher flux measurements, in-situ pump, and CTD particulate data, we show that for a large part of the productive season, diatoms do not represent efficient vectors of sinking POC through the mesopelagic, yet POC is still efficiently transferred to depth. We suggest that processes influencing flux attenuation differ between the upper mesopelagic and deep ocean, with rapid BSi flux attenuation in the upper mesopelagic caused by elevated rates of BSi remineralization or negation of biomineral ballast effects by particle processes such as buoyancy regulation or fragmentation. Biomineral ballast may yet play an important role in shaping the efficiency of sinking POC transfer in the deep ocean. More broadly, these results highlight the need to understand the nuanced role this key taxon plays in transferring carbon through the mesopelagic, a region that is highly vulnerable to climate change effects and key in shaping the efficiency of downward carbon transport. As diatoms appear to be inefficient at delivering carbon to the deep ocean, projected losses in the strength of the Southern Ocean BCP due to shifts in phytoplankton community composition to smaller size classes may be less than previously predicted.

The Southern Ocean, a region highly vulnerable to climate change, plays a vital role in regulating global nutrient cycles and atmospheric CO2 via the biological carbon pump. Diatoms, photosynthetically active plankton with dense opal skeletons, are key to this process as their exoskeletons are thought to enhance the transfer of particulate organic carbon to depth, positioning them as major vectors of carbon storage. Yet conflicting observations obscure the mechanistic link between diatoms, opal and particulate organic carbon fluxes, especially in the twilight zone where greatest flux losses occur. Here we present direct springtime flux measurements from different sectors of the subpolar Southern Ocean, demonstrating that across large areas of the subpolar twilight zone, carbon is efficiently transferred to depth, albeit not by diatoms. Rather, opal is retained near the surface ocean, indicating that processes such as diatom buoyancy regulation and grazer repackaging can negate ballast effects of diatoms’ skeletons. Our results highlight that the presence of diatoms in surface waters of the Southern Ocean’s largest biome does not guarantee their importance as vectors for efficient carbon transfer through the subpolar twilight zone. Climate change-driven shifts in phytoplankton community composition may affect biologically sequestered carbon pools less than currently predicted. Diatom skeletons largely remain near the surface of the subpolar Southern Ocean following diatom bloom events, suggesting that they do not play as big a role in the downward flux of organic matter as previously thought, according to data from two expeditions focused on the marine twilight zone.

Diazotrophs regulate marine productivity in the oligotrophic ocean by alleviating nitrogen limitation, contributing to particulate organic carbon (POC) export to the deep ocean. Yet, the characterization of particles composing the sinking POC flux has never been explored in such ecosystems. Moreover, the contribution of the direct gravitational export of diazotrophs to the overall flux is seldom assessed. Here we explore the composition of the sinking POC flux in a hot spot of N2 fixation (the western sub-tropical South Pacific) using polyacrylamide gel-filled traps deployed at two stations (S05M and S10M) and three depths (170 m, 270 m, 1000 m) during the TONGA expedition (November-December 2019). Image analyses of particles collected in the gels was used to classify them into 5 categories (fecal aggregates, phytodetrital aggregates, mixed aggregates, cylindrical fecal pellets, and zooplankton carcasses). Fecal aggregates were the most abundant at both stations and all depths and dominated the flux (average of 56 ± 28% of the POC flux), followed by zooplankton carcasses (24 ± 19%), cylindrical fecal pellets (15 ± 14%) and mixed aggregates (5 ± 4%), whereas phytodetrital aggregates contributed less (<1%). Since N isotope budgets show that export is mainly supported by diazotrophy at these stations, these results suggest that the diazotroph-derived N has been efficiently transferred to the foodweb up to zooplankton and fecal pellets before being exported, pleading for an indirect export of diazotrophy. However, random confocal microscopy examination performed on sinking particles revealed that diazotrophs were present in several categories of exported particles, suggesting that diazotrophs are also directly exported, with a potential contribution to overall POC fluxes increasing with depth. Our results provide the first characterization of particle categories composing the sinking flux and their contribution to the overall flux in a hot spot of N2 fixation.

The ocean–atmosphere exchange of carbon largely depends on the balance between carbon export of particulate organic carbon (POC) as sinking marine particles, and POC remineralization by attached microbial communities. Despite the vast spectrum of types, sources, ages, shapes, and composition of individual sinking particles, they are usually considered as a bulk together with their associated microbial communities. This limits our mechanistic understanding of the biological carbon pump (BCP) and its feedback on the global carbon cycle. We established a method to sample individual particles while preserving their shape, structure, and nucleic acids by placing a jellified RNA‐fixative at the bottom of drifting sediment traps. Coupling imaging of individual particles with associated 16S rRNA analysis reveals that active bacterial communities are highly heterogenous from one particles origin to another. In contrast to lab‐made particles, we found that complex in situ conditions lead to heterogeneity even within the same particle type. Our new method allows to associate patterns of active prokaryotic and functional diversity to particle features, enabling the detection of potential remineralization niches. This new approach will therefore improve our understanding of the BCP and numerical representation in the context of a rapidly changing ocean.

The gravitational sinking of organic debris from ocean ecosystems is a dominant mechanism of the biological carbon pump (BCP) that regulates the global climate. The fraction of primary production exported downward, the e‐ratio, is an important but poorly constrained BCP metric. In mid‐ and high‐latitude oceans, seasonal and local variations of sinking particle fluxes strongly modulate the e‐ratio. These locally specific e‐ratio variations and their ecological foundations are here encapsulated in the term “export systems” (ES). ES have been partly characterized for a few ocean locations but remain largely ignored over most of the ocean surface. Here, in a fully conceptual approach and with the primary aim to understand rather than to estimate ocean carbon export, we combine biogeochemical (BGC) modeling with satellite observations to map ES at fine spatio‐temporal scales. We identify four plausible ES with distinct e‐ratio seasonalities across mid‐ and high‐latitude oceans. The ES map confirms the outlines of traditional BGC provinces and unveils new boundaries indicating where (and how) the annual relationship between carbon export and production changes markedly. At six sites where ES features can be partially inferred from in situ data, we test our approach and propose key ecological processes driving carbon export. In the light of our findings, a re‐examination of 1,841 field‐based e‐ratios could challenge the conventional wisdom that e‐ratios change strongly with latitude, suggesting a possible seasonal artifact caused by the timing of observations. By deciphering carbon export mechanistically, our conceptual ES map provides timely directions to emergent ocean robotic explorations of the BCP.

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.

Determining mesopelagic organic carbon budgets is essential to characterize the ocean's role as a carbon dioxide sink. This is because the biological processes observed in the mesopelagic zone are crucial for understanding the biological carbon pump. Yet, field assessments of carbon budgets are often unbalanced with the carbon demand exceeding its supply. This underlines either methodological issues in the budget calculations or incomplete knowledge of the mesopelagic carbon cycling with potentially missing sources. Carbon budgets are built by partitioning the ocean into vertical depth zones. Vertical boundaries are conventionally defined between 200 and 1000 m depth or using various thresholds. Such approaches lack consistent methodology preventing robust comparison of mesopelagic carbon budget from region to region. Here, using a statistical rupture detection method applied to conductivity-temperature-depth (CTD)-cast variables (fluorescence, O-2 concentration, potential temperature, salinity, and density), we aim to provide independent estimates of mesopelagic boundaries. We demonstrate that the so-determined upper boundary is highly correlated with the knee points of the particulate organic carbon (POC) fluxes estimated by a power law and that over 90% of the POC flux attenuation occurs within our method boundaries. The identified zone therefore corresponds to the most active part of the conventional mesopelagic zone and we name it the "active mesopelagic zone" (AMZ). We find that the depths of the mesopelagic zone depend on the region considered. Our results demonstrate that the mesopelagic carbon budget discrepancy can vary up to four folds depending on the boundaries chosen and hence provide novel grounds to reassess existing and future mesopelagic carbon budgets.

In the ocean, downward flux of particles produced in sunlit surface waters is the major component of the biological carbon pump, which sequesters atmospheric carbon dioxide and fuels deep-sea ecosystems. The efficiency of downward carbon transfer is expected to be particularly high in tropical upwelling systems where hypoxia occurring beneath the productive surface waters is thought to hamper particle consumption. However, observations of both particle feeders and carbon export in low-oxygen waters are scarce. Here, we provide evidence that hypoxia-tolerant zooplankton feed on sinking particles in the extensive Oxygen Minimum Zone (OMZ) off Peru. Using several arrays of drifting sediment traps and in situ imaging, we show geochemical and morphological transformations of sinking particles and substantial control of carbon export by zooplankton. Our findings challenge the assumption of a consistently efficient biological carbon pump in OMZs and further demonstrate the need to consider mesopelagic organisms when studying oceanic carbon sequestration.

The transfer of photosynthetically produced organic carbon from surface to mesopelagic waters draws carbon dioxide from the atmosphere(1). However, current observation-based estimates disagree on the strength of this biological carbon pump (BCP)(2). Earth system models (ESMs) also exhibit a large spread of BCP estimates, indicating limited representations of the known carbon export pathways(3). Here we use several decades of hydrographic observations to produce a top-down estimate of the strength of the BCP with an inverse biogeochemical model that implicitly accounts for all known export pathways. Our estimate of total organic carbon (TOC) export at 73.4 m (model euphotic zone depth) is 15.00 +/- 1.12 Pg C year(-1), with only two-thirds reaching 100 m depth owing to rapid remineralization of organic matter in the upper water column. Partitioned by sequestration time below the euphotic zone, tau, the globally integrated organic carbon production rate with tau > 3 months is 11.09 +/- 1.02 Pg C year(-1), dropping to 8.25 +/- 0.30 Pg C year(-1) for tau > 1 year, with 81% contributed by the non-advective-diffusive vertical flux owing to sinking particles and vertically migrating zooplankton. Nevertheless, export of organic carbon by mixing and other fluid transport of dissolved matter and suspended particles remains regionally important for meeting the respiratory carbon demand. Furthermore, the temperature dependence of the sequestration efficiency inferred from our inversion suggests that future global warming may intensify the recycling of organic matter in the upper ocean, potentially weakening the BCP.

Through the constant rain of sinking marine particles in the ocean, carbon (C) trapped within is exported into the water column and sequestered when reaching depths below the mesopelagic zone. Atmospheric CO2 levels are thereby strongly related to the magnitude of carbon export fluxes in the mesopelagic zone. Sinking particles represent the main source of carbon and energy for mesopelagic organisms, attenuating the C export flux along the water column. Attempts to quantify the amount of C exported versus C consumed by heterotrophic organisms have increased in recent decades. Yet, most of the conducted estimations have led to estimated C demands several times higher than the measured C export fluxes. The choice of parameters such as growth efficiencies or various conversion factors is known to greatly impact the resulting C budget. In parallel, field or experimental data are sorely lacking to obtain accurate values of these crucial overlooked parameters. In this study, we identify the most influential of these parameters and perform inversion of a mechanistic model. Further, we determine the optimal parameter values as the ones that best explain the observed prokaryotic respiration, prokaryotic production and zooplankton respiration. The consistency of the resulting C budget suggests that such budgets can be adequately balanced when using appropriate parameters.

Diazotrophs are ubiquitous in the surface (sub)tropical ocean, where they sustain most new primary production. Several recent studies also report the presence of diverse cyanobacterial diazotrophs in the mesopelagic and bathypelagic ocean, suggesting that they gravitationally sink, potentially supporting organic matter export and the biological carbon pump. Yet, the mechanisms leading to their export are not elucidated. Here, we simulated the sinking of diazotrophs in the water column by using rolling tanks, and measured the aggregation capacity and sinking velocities of four globally distributed strains having different sizes, shapes, and abilities to produce transparent exopolymer particles (TEP): two filamentous diazotrophs (Trichodesmium erythraeum, Calothrix sp.) and two unicellular cyanobacterial diazotrophs (UCYN-B, Crocosphaera watsonii) and (UCYN-C, Cyanothece sp.). All diazotrophs tested, regardless their size and shape, were capable of forming aggregates and sunk, albeit at different velocities depending on the aggregation capacity. Overall, UCYN formed aggregates as large as those formed by the filamentous diazotrophs (7000-32,014 mu m ESD, equivalent spherical diameter), and sunk at 100-400 m d(-1), i.e., at the same velocity as filamentous diazotrophs (92-400 m d(-1)). Although TEP are generally considered as enhancers of aggregation, TEP did not clearly influence aggregation rates nor sinking velocities during our study. We conclude that diazotrophs may be important contributors to carbon export in the ocean and need to be considered in future studies to improve the accuracy of current regional and global estimates of export.

Iron is an essential nutrient that regulates productivity in ~30% of the ocean. Compared with deep (>2000 meter) hydrothermal activity at mid-ocean ridges that provide iron to the ocean's interior, shallow (<500 meter) hydrothermal fluids are likely to influence the surface's ecosystem. However, their effect is unknown. In this work, we show that fluids emitted along the Tonga volcanic arc (South Pacific) have a substantial impact on iron concentrations in the photic layer through vertical diffusion. This enrichment stimulates biological activity, resulting in an extensive patch of chlorophyll (360,000 square kilometers). Diazotroph activity is two to eight times higher and carbon export fluxes are two to three times higher in iron-enriched waters than in adjacent unfertilized waters. Such findings reveal a previously undescribed mechanism of natural iron fertilization in the ocean that fuels regional hotspot sinks for atmospheric CO2.

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.

Together with T–S properties, particle abundance in situ measurements are useful to discriminate water masses and derive circulation patterns. In the upper layers of the Ionian Sea, the fresher Atlantic Waters (AW) recently crossing the Sicily Channel meet the resident and saltier AW, which circulated cyclonically in the eastern basin and modified after evaporation and eventually cooling. In May 2017, during the PEACETIME cruise, fluorescence and particle abundance sampled at high resolution revealed unexpected heterogeneity in the central Ionian Sea. Surface salinity measurements, together with altimetry-derived and hull-mounted acoustic Doppler current profiler (ADCP) currents, describe a zonal pathway of AW entering the Ionian Sea, consistent with the so-called cyclonic mode in the North Ionian Gyre. The ION-Tr transect, located between 19–20∘ E at approximately 36∘ N, turned out to be at the crossroads of three water masses, mostly coming from the west, north and an isolated anticyclonic eddy northeast of ION-Tr. Using Lagrangian numerical simulations, we suggest that the contrast in particle loads along ION-Tr originates from particles transported from these three different water masses. Waters from the west, identified as AW carried by a strong southwestward jet, were moderate in particle load, probably originating from the Sicily Channel. The water mass from the north, carrying abundant particles, probably originated in the northern Ionian Sea, or further away from the south Adriatic Sea. Waters from the eddy, depleted in particles and chl a, may originate from south of the Peloponnese, where the Pelops eddy forms. The central Ionian Sea hence appears as a mosaic area, where waters of contrasted biological history meet. This contrast is particularly clear in spring, when blooming and non-blooming areas co-occur. Interpreting the complex dynamics of physical–biogeochemical coupling from discrete measurements made at isolated stations at sea is a challenge. The combination of multiparametric in situ measurements at high resolution with remote sensing and Lagrangian modeling appears as one adequate way to address this challenge.