Release of ballast material during sea-ice melt enhances carbon export in the Arctic Ocean.

Globally, the most intense uptake of anthropogenic carbon dioxide (CO2) occurs in the Atlantic north of 50°N, and it has been predicted that atmospheric CO2 sequestration in the Arctic Ocean will increase as a result of ice-melt and increased primary production. However, little is known about the impact of pan-Arctic sea-ice decline on carbon export processes. We investigated the potential ballasting effect of sea-ice derived material on settling aggregates and carbon export in the Fram Strait by combining 13 years of vertical flux measurements with benthic eDNA analysis, laboratory experiments, and tracked sea-ice distributions. We show that melting sea-ice in the Fram Strait releases cryogenic gypsum and terrigenous material, which ballasts sinking organic aggregates. As a result, settling velocities of aggregates increased ≤10-fold, resulting in ≤30% higher carbon export in the vicinity of the melting ice-edge. Cryogenic gypsum is formed in first-year sea-ice, which is predicted to increase as the Arctic is warming. Simultaneously, less sea-ice forms over the Arctic shelves, which is where terrigenous material is incorporated into sea-ice. Supporting this, we found that terrigenous fluxes from melting sea-ice in the Fram Strait decreased by >80% during our time-series. Our study suggests that terrigenous flux will eventually cease when enhanced sea-ice melt disrupts trans-Arctic sea-ice transport and thus, limit terrigenous-ballasted carbon flux. However, the predicted increase in Arctic primary production and gypsum formation may enhance gypsum-ballasted carbon flux and compensate for lowered terrigenous fluxes. It is thus unclear if sea-ice loss will reduce carbon export in the Arctic Ocean.

Iron and manganese availability drives primary production and carbon export in the Weddell Sea.

Next to iron (Fe), recent phytoplankton-enrichment experiments identified manganese (Mn) to (co-)limit Southern Ocean phytoplankton biomass and species composition. Since taxonomic diversity affects aggregation time and sinking rate, the efficiency of the biological carbon pump is directly affected by community structure. However, the impact of FeMn co-limitation on Antarctic primary production, community composition, and the subsequent export of carbon to depth requires more investigation. In situ samplings of 6 stations in the understudied southern Weddell Sea revealed that surface Fe and Mn concentrations, primary production, and carbon export rates were all low, suggesting a FeMn co-limited phytoplankton community. An Fe and Mn addition experiment examined how changes in the species composition drive the aggregation capability of a natural phytoplankton community. Primary production rates were highest when Fe and Mn were added together, due to an increased abundance of the colonial prymnesiophyte Phaeocystis antarctica. Although the community remained diatom dominated, the increase in Phaeocystis abundance led to highly carbon-enriched aggregates and a 4-fold increase in the carbon export potential compared to the control, whereas it only doubled in the Fe treatment. Based on the outcome of the FeMn-enrichment experiment, this region may suffer from FeMn co-limitation. As the Weddell Sea represents one of the most productive Antarctic marginal ice zones, our findings highlight that in response to greater Fe and Mn supply, changes in plankton community composition and primary production can have a disproportionally larger effect on the carbon export potential.

Fungal parasitism on diatoms alters formation and bio-physical properties of sinking aggregates.

Phytoplankton forms the base of aquatic food webs and element cycling in diverse aquatic systems. The fate of phytoplankton-derived organic matter, however, often remains unresolved as it is controlled by complex, interlinked remineralization and sedimentation processes. We here investigate a rarely considered control mechanism on sinking organic matter fluxes: fungal parasites infecting phytoplankton. We demonstrate that bacterial colonization is promoted 3.5-fold on fungal-infected phytoplankton cells in comparison to non-infected cells in a cultured model pathosystem (diatom Synedra, fungal microparasite Zygophlyctis, and co-growing bacteria), and even ≥17-fold in field-sampled populations (Planktothrix, Synedra, and Fragilaria). Additional data obtained using the Synedra-Zygophlyctis model system reveals that fungal infections reduce the formation of aggregates. Moreover, carbon respiration is 2-fold higher and settling velocities are 11-48% lower for similar-sized fungal-infected vs. non-infected aggregates. Our data imply that parasites can effectively control the fate of phytoplankton-derived organic matter on a single-cell to single-aggregate scale, potentially enhancing remineralization and reducing sedimentation in freshwater and coastal systems.

Carbon Export in the Ocean: A Biologist's Perspective.

Understanding the nature of organic matter flux in the ocean remains a major goal of oceanography because it impacts some of the most important processes in the ocean. Sinking particles are important for carbon dioxide removal from the atmosphere and its movement to the deep ocean. They also feed life below the ocean's productive surface and sustain life in the deep sea, in addition to depositing organic matter on the seafloor. However, the magnitude of all of these processes is dependent on the transformation of sinking particles during their journey through the water column. This review focuses on the movement of organic matter from the surface ocean to the deep sea via the biological carbon pump and examines the processes that prevent this downward movement-namely, attenuation via microbial colonization and zooplankton feeding. It also discusses how the depth-specific interactions among microbes, zooplankton, and aggregates determine carbon export as well as nutrient recycling, which in turn impact ocean production and Earth's climate.

Machine learning techniques to characterize functional traits of plankton from image data.

Plankton imaging systems supported by automated classification and analysis have improved ecologists' ability to observe aquatic ecosystems. Today, we are on the cusp of reliably tracking plankton populations with a suite of lab-based and in situ tools, collecting imaging data at unprecedentedly fine spatial and temporal scales. But these data have potential well beyond examining the abundances of different taxa; the individual images themselves contain a wealth of information on functional traits. Here, we outline traits that could be measured from image data, suggest machine learning and computer vision approaches to extract functional trait information from the images, and discuss promising avenues for novel studies. The approaches we discuss are data agnostic and are broadly applicable to imagery of other aquatic or terrestrial organisms.

Efficient carbon and nitrogen transfer from marine diatom aggregates to colonizing bacterial groups.

Bacterial degradation of sinking diatom aggregates is key for the availability of organic matter in the deep-ocean. Yet, little is known about the impact of aggregate colonization by different bacterial taxa on organic carbon and nutrient cycling within aggregates. Here, we tracked the carbon (C) and nitrogen (N) transfer from the diatom Leptocylindrus danicus to different environmental bacterial groups using a combination of 13C and 15N isotope incubation (incubated for 72 h), CARD-FISH and nanoSIMS single-cell analysis. Pseudoalteromonas bacterial group was the first colonizing diatom-aggregates, succeeded by the Alteromonas group. Within aggregates, diatom-attached bacteria were considerably more enriched in 13C and 15N than non-attached bacteria. Isotopic mass balance budget indicates that both groups showed comparable levels of diatom C in their biomass, accounting for 19 ± 7% and 15 ± 11%, respectively. In contrast to C, bacteria of the Alteromonas groups showed significantly higher levels of N derived from diatoms (77 ± 28%) than Pseudoalteromonas (47 ± 17%), suggesting a competitive advantage for Alteromonas in the N-limiting environments of the deep-sea. Our results imply that bacterial succession within diatom aggregates may largely impact taxa-specific C and N uptake, which may have important consequences for the quantity and quality of organic matter exported to the deep ocean.

Krill and salp faecal pellets contribute equally to the carbon flux at the Antarctic Peninsula.

Krill and salps are important for carbon flux in the Southern Ocean, but the extent of their contribution and the consequences of shifts in dominance from krill to salps remain unclear. We present a direct comparison of the contribution of krill and salp faecal pellets (FP) to vertical carbon flux at the Antarctic Peninsula using a combination of sediment traps, FP production, carbon content, microbial degradation, and krill and salp abundances. Salps produce 4-fold more FP carbon than krill, but the FP from both species contribute equally to the carbon flux at 300 m, accounting for 75% of total carbon. Krill FP are exported to 72% to 300 m, while 80% of salp FP are retained in the mixed layer due to fragmentation. Thus, declining krill abundances could lead to decreased carbon flux, indicating that the Antarctic Peninsula could become a less efficient carbon sink for anthropogenic CO2 in future.

Sea-ice derived meltwater stratification slows the biological carbon pump: results from continuous observations.

The ocean moderates the world's climate through absorption of heat and carbon, but how much carbon the ocean will continue to absorb remains unknown. The North Atlantic Ocean west (Baffin Bay/Labrador Sea) and east (Fram Strait/Greenland Sea) of Greenland features the most intense absorption of anthropogenic carbon globally; the biological carbon pump (BCP) contributes substantially. As Arctic sea-ice melts, the BCP changes, impacting global climate and other critical ocean attributes (e.g. biodiversity). Full understanding requires year-round observations across a range of ice conditions. Here we present such observations: autonomously collected Eulerian continuous 24-month time-series in Fram Strait. We show that, compared to ice-unaffected conditions, sea-ice derived meltwater stratification slows the BCP by 4 months, a shift from an export to a retention system, with measurable impacts on benthic communities. This has implications for ecosystem dynamics in the future warmer Arctic where the seasonal ice zone is expected to expand.

Sea ice presence is linked to higher carbon export and vertical microbial connectivity in the Eurasian Arctic Ocean.

Arctic Ocean sea ice cover is shrinking due to warming. Long-term sediment trap data shows higher export efficiency of particulate organic carbon in regions with seasonal sea ice compared to regions without sea ice. To investigate this sea-ice enhanced export, we compared how different early summer phytoplankton communities in seasonally ice-free and ice-covered regions of the Fram Strait affect carbon export and vertical dispersal of microbes. In situ collected aggregates revealed two-fold higher carbon export of diatom-rich aggregates in ice-covered regions, compared to Phaeocystis aggregates in the ice-free region. Using microbial source tracking, we found that ice-covered regions were also associated with more surface-born microbial clades exported to the deep sea. Taken together, our results showed that ice-covered regions are responsible for high export efficiency and provide strong vertical microbial connectivity. Therefore, continuous sea-ice loss may decrease the vertical export efficiency, and thus the pelagic-benthic coupling, with potential repercussions for Arctic deep-sea ecosystems.

Selective feeding in Southern Ocean key grazers-diet composition of krill and salps.

Over the past decades, two key grazers in the Southern Ocean (SO), krill and salps, have experienced drastic changes in their distribution and abundance, leading to increasing overlap of their habitats. Both species occupy different ecological niches and long-term shifts in their distributions are expected to have cascading effects on the SO ecosystem. However, studies directly comparing krill and salps are lacking. Here, we provide a direct comparison of the diet and fecal pellet composition of krill and salps using 18S metabarcoding and fatty acid markers. Neither species' diet reflected the composition of the plankton community, suggesting that in contrast to the accepted paradigm, not only krill but also salps are selective feeders. Moreover, we found that krill and salps had broadly similar diets, potentially enhancing the competition between both species. This could be augmented by salps' ability to rapidly reproduce in favorable conditions, posing further risks to krill populations.

Salp fecal pellets release more bioavailable iron to Southern Ocean phytoplankton than krill fecal pellets.

Over the last decades, it has been reported that the habitat of the Southern Ocean (SO) key species Antarctic krill (Euphausia superba) has contracted to high latitudes, putatively due to reduced winter sea ice coverage, while salps as Salpa thompsoni have extended their dispersal to the former krill habitats. To date, the potential implications of this population shift on the biogeochemical cycling of the limiting micronutrient iron (Fe) and its bioavailability to SO phytoplankton has never been tested. Based on uptake of fecal pellet (FP)-released Fe by SO phytoplankton, this study highlights how efficiently krill and salps recycle Fe. To test this, we collected FPs of natural populations of salps and krill, added them to the same SO phytoplankton community, and measured the community's Fe uptake rates. Our results reveal that both FP additions yielded similar dissolved iron concentrations in the seawater. Per FP carbon added to the seawater, 4.8 ± 1.5 times more Fe was taken up by the same phytoplankton community from salp FP than from krill FP, suggesting that salp FP increased the Fe bioavailability, possibly through the release of ligands. With respect to the ongoing shift from krill to salps, the potential for carbon fixation of the Fe-limited SO could be strengthened in the future, representing a negative feedback to climate change.

Small sinking particles control anammox rates in the Peruvian oxygen minimum zone.

Anaerobic oxidation of ammonium (anammox) in oxygen minimum zones (OMZs) is a major pathway of oceanic nitrogen loss. Ammonium released from sinking particles has been suggested to fuel this process. During cruises to the Peruvian OMZ in April-June 2017 we found that anammox rates are strongly correlated with the volume of small particles (128-512 µm), even though anammox bacteria were not directly associated with particles. This suggests that the relationship between anammox rates and particles is related to the ammonium released from particles by remineralization. To investigate this, ammonium release from particles was modelled and theoretical encounters of free-living anammox bacteria with ammonium in the particle boundary layer were calculated. These results indicated that small sinking particles could be responsible for ~75% of ammonium release in anoxic waters and that free-living anammox bacteria frequently encounter ammonium in the vicinity of smaller particles. This indicates a so far underestimated role of abundant, slow-sinking small particles in controlling oceanic nutrient budgets, and furthermore implies that observations of the volume of small particles could be used to estimate N-loss across large areas.

Laminarin is a major molecule in the marine carbon cycle.

Marine microalgae sequester as much CO2 into carbohydrates as terrestrial plants. Polymeric carbohydrates (i.e., glycans) provide carbon for heterotrophic organisms and constitute a carbon sink in the global oceans. The quantitative contributions of different algal glycans to cycling and sequestration of carbon remain unknown, partly because of the analytical challenge to quantify glycans in complex biological matrices. Here, we quantified a glycan structural type using a recently developed biocatalytic strategy, which involves laminarinase enzymes that specifically cleave the algal glycan laminarin into readily analyzable fragments. We measured laminarin along transects in the Arctic, Atlantic, and Pacific oceans and during three time series in the North Sea. These data revealed a median of 26 ± 17% laminarin within the particulate organic carbon pool. The observed correlation between chlorophyll and laminarin suggests an annual production of algal laminarin of 12 ± 8 gigatons: that is, approximately three times the annual atmospheric carbon dioxide increase by fossil fuel burning. Moreover, our data revealed that laminarin accounted for up to 50% of organic carbon in sinking diatom-containing particles, thus substantially contributing to carbon export from surface waters. Spatially and temporally variable laminarin concentrations in the sunlit ocean are driven by light availability. Collectively, these observations highlight the prominent ecological role and biogeochemical function of laminarin in oceanic carbon export and energy flow to higher trophic levels.

Microbial communities in the nepheloid layers and hypoxic zones of the Canary Current upwelling system.

Eastern boundary upwelling systems (EBUSs) are among the most productive marine environments in the world. The Canary Current upwelling system off the coast of Mauritania and Morocco is the second most productive of the four EBUS, where nutrient-rich waters fuel perennial phytoplankton blooms, evident by high chlorophyll a concentrations off Cape Blanc, Mauritania. High primary production leads to eutrophic waters in the surface layers, whereas sinking phytoplankton debris and horizontally dispersed particles form nepheloid layers (NLs) and hypoxic waters at depth. We used Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (CARD-FISH) in combination with fatty acid (measured as methyl ester; FAME) profiles to investigate the bacterial and archaeal community composition along transects from neritic to pelagic waters within the "giant Cape Blanc filament" in two consecutive years (2010 and 2011), and to evaluate the usage of FAME data for microbial community studies. We also report the first fatty acid profile of Pelagibacterales strain HTCC7211 which was used as a reference profile for the SAR11 clade. Unexpectedly, the reference profile contained low concentrations of long chain fatty acids 18:1 cis11, 18:1 cis11 11methyl, and 19:0 cyclo11-12 fatty acids, the main compounds in other Alphaproteobacteria. Members of the free-living SAR11 clade were found at increased relative abundance in the hypoxic waters in both years. In contrast, the depth profiles of Gammaproteobacteria (including Alteromonas and Pseudoalteromonas), Bacteroidetes, Roseobacter, and Synechococcus showed high abundances of these groups in layers where particle abundance was high, suggesting that particle attachment or association is an important mechanisms of dispersal for these groups. Collectively, our results highlight the influence of NLs, horizontal particle transport, and low oxygen on the structure and dispersal of microbial communities in upwelling systems.

Environmental Drivers of Free-Living vs. Particle-Attached Bacterial Community Composition in the Mauritania Upwelling System.

Saharan dust input and seasonal upwelling along North-West Africa provide a model system for studying microbial processes related to the export and recycling of nutrients. This study offers the first molecular characterization of prokaryotic particle-attached (PA; >3.0 µm) and free-living (FL; 0.2-3.0 µm) players in this important ecosystem during August 2016. Environmental drivers for alpha-diversity, bacterial community composition, and differences between FL and PA fractions were identified. The ultra-oligotrophic waters off Senegal were dominated by Cyanobacteria while higher relative abundances of Alphaproteobacteria, Bacteroidetes, Verrucomicrobia, and Planctomycetes (known particle-degraders) occurred in the upwelling area. Temperature, proxy for different water masses, was the best predictor for changes in FL communities. PA community variation was best explained by temperature and ammonium. Bray Curtis dissimilarities between FL and PA were generally very high and correlated with temperature and salinity in surface waters. Greatest similarities between FL and PA occurred at the deep chlorophyll maximum, where bacterial substrate availability was likely highest. This indicates that environmental drivers do not only influence changes among FL and PA communities but also differences between them. This could provide an explanation for contradicting results obtained by different studies regarding the dissimilarity/similarity between FL and PA communities and their biogeochemical functions.

A new mathematical model to explore microbial processes and their constraints in phytoplankton colonies and sinking marine aggregates.

N2-fixing colonies of cyanobacteria and aggregates of phytoplankton and detritus sinking hundreds of meters per day are instrumental for the ocean's sequestration of CO2 from the atmosphere. Understanding of small-scale microbial processes associated with phytoplankton colonies and aggregates is therefore crucial for understanding large-scale biogeochemical processes in the ocean. Phytoplankton colonies and sinking aggregates are characterized by steep concentration gradients of gases and nutrients in their interior. Here, we present a mechanistic mathematical model designed to perform modeling of small-scale fluxes and evaluate the physical, chemical, and biological constraints of processes that co-occur in phytoplankton colonies and sinking porous aggregates. The model accurately reproduced empirical measurements of O2 concentrations and fluxes measured in sinking aggregates. Common theoretical assumptions of either constant concentration or constant flux over the entire surface did not apply to sinking aggregates. Consequently, previous theoretical models overestimate O2 flux in these aggregates by as high as 15-fold.

Limited sinking of Phaeocystis during a 12 days sediment trap study.

There is a controversy discussion about the contribution of the genus Phaeocystis to the vertical carbon export with evidence for and against sedimentation of Phaeocystis. So far, the presence of Phaeocystis in sinking matter was investigated with methods depending on morphological features (microscopy) and fast degradable substances (biochemical analyses). In this study, we determine the occurrence and abundance of Phaeocystis antarctica in short-term sediment traps and the overlying water column during a 12-day time period in the Atlantic sector of the Southern Ocean with 454-pyrosequencing and microscopy counting. In the sediment trap samples, we only found few sequences belonging to Phaeocystis, which was not reflecting the situation in the water column above. The cell counts showed the same results. We conclude that Phaeocystis cells are not generally transported downwards by active sinking or other sinking processes.

Colonization in the photic zone and subsequent changes during sinking determine bacterial community composition in marine snow.

Due to sampling difficulties, little is known about microbial communities associated with sinking marine snow in the twilight zone. A drifting sediment trap was equipped with a viscous cryogel and deployed to collect intact marine snow from depths of 100 and 400 m off Cape Blanc (Mauritania). Marine snow aggregates were fixed and washed in situ to prevent changes in microbial community composition and to enable subsequent analysis using catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH). The attached microbial communities collected at 100 m were similar to the free-living community at the depth of the fluorescence maximum (20 m) but different from those at other depths (150, 400, 550, and 700 m). Therefore, the attached microbial community seemed to be "inherited" from that at the fluorescence maximum. The attached microbial community structure at 400 m differed from that of the attached community at 100 m and from that of any free-living community at the tested depths, except that collected near the sediment at 700 m. The differences between the particle-associated communities at 400 m and 100 m appeared to be due to internal changes in the attached microbial community rather than de novo colonization, detachment, or grazing during the sinking of marine snow. The new sampling method presented here will facilitate future investigations into the mechanisms that shape the bacterial community within sinking marine snow, leading to better understanding of the mechanisms which regulate biogeochemical cycling of settling organic matter.

Ecological structuring of bacterial and archaeal taxa in surface ocean waters.

The Global Ocean Sampling (GOS) expedition is currently the largest and geographically most comprehensive metagenomic dataset, including samples from the Atlantic, Pacific, and Indian Oceans. This study makes use of the wide range of environmental conditions and habitats encompassed within the GOS sites in order to investigate the ecological structuring of bacterial and archaeal taxon ranks. Community structures based on taxonomically classified 16S ribosomal RNA (rRNA) gene fragments at phylum, class, order, family, and genus rank levels were examined using multivariate statistical analysis, and the results were inspected in the context of oceanographic environmental variables and structured habitat classifications. At all taxon rank levels, community structures of neritic, oceanic, estuarine biomes, as well as other exotic biomes (salt marsh, lake, mangrove), were readily distinguishable from each other. A strong structuring of the communities with chlorophyll a concentration and a weaker yet significant structuring with temperature and salinity were observed. Furthermore, there were significant correlations between community structures and habitat classification. These results were used for further investigation of one-to-one relationships between taxa and environment and provided indications for ecological preferences shaped by primary production for both cultured and uncultured bacterial and archaeal clades.