Unveiling pelagic-benthic coupling associated with the biological carbon pump in the Fram Strait (Arctic Ocean)

Abstract

Settling aggregates transport organic matter from the ocean surface to the deep sea and seafloor. Though plankton communities impact carbon export, how specific organisms and their interactions affect export efficiency is unknown. Looking at 15 years of eDNA sequences (18S-V4) from settling and sedimented organic matter in the Fram Strait, here we observe that most phylogenetic groups were transferred from pelagic to benthic ecosystems. Chaetoceros socialis, sea-ice diatoms, Radiolaria, and Chaetognatha are critical components of vertical carbon flux to 200 m depth. In contrast, the diatom C. socialis alone is essential for the amount of organic carbon reaching the seafloor. Spatiotemporal changes in community composition show decreasing diatom abundance during warm anomalies, which would reduce the efficiency of a diatom-driven biological carbon pump. Interestingly, several parasites are also tightly associated with carbon flux and show a strong vertical connectivity, suggesting a potential role in sedimentation processes involving their hosts, especially through interactions with resting spores, which could have implications for pelagic-benthic coupling and overall ecosystem functioning.

Fig. 1. Overview of sampling sites.

a Map of the Long-term Ecological Research (LTER) observatory HAUSGARTEN in the Fram Strait and b detail of the longitudinal bathymetric transect from the stations HG-I to HG-IX. The upper water column was sampled at the central station (HG-IV), and the sediment cores were performed at all HG stations. The abbreviations S, N, EG, and HG refer to the South, North, East Greenland, and HAUSGARTEN sampling areas, respectively. The red dots refer to the sampling stations. The red and blue arrows indicate the West Spitsbergen Current (WSC) and the East Greenland Current (EGC) trajectories.

Fig. 2. Visualization of the pelagic subnetwork features identified by the WGCNA method.

a Pearson correlations between each subnetwork and the environmental data. b Relative abundance of the main orders in each subnetwork. c Inter- and intra-annual changes of subnetworks contribution at the central HAUSGARTEN Observatory. Zooplankton and biogeochemical fluxes (including total particulate matter, POC, PON, bPSi, CaCO3, ∂13 C, and ∂15 N) were estimated from sediment traps. Sinkers (i.e., zooplankton passively sink into the trap) and swimmers (i.e., zooplankton actively swam into the trap) larger than 0.5 mm were individually picked, rinsed, identified, and counted under microscope. All environmental variables (such as NAO for North Atlantic Oscillation, AO for Arctic Oscillation, AMO for Atlantic Multidecadal Oscillation, and ‘u’ and ‘v’ representing the east–west and north–south components of wind, current, and sea-ice velocity, respectively) included in the correlogram were described in Ramondenc et al.. The colors corresponding to each subnetwork (Sn) are consistent across the subplots.

Fig. 3. Key taxonomic lineages linked to the carbon cycle at the HAUSGARTEN observatory.

Lineages identification is provided for a the pelagic carbon flux and b benthic carbon content in the Fram Strait associated with c a Venn diagram showing the number of families shared between subnetworks of interest. The degree centrality highlights nodes with the most direct connections, whereas dot color and size represent, respectively, the VIP score in the PLS analyses and taxonomy assigned to the ASVs.

Fig. 4. Visualization of the benthic subnetwork features identified by the WGCNA method.

a Pearson correlation between each subnetwork and the environmental data. b Relative abundance of the main orders in each subnetwork. c Spatiotemporal changes of subnetworks contribution at the HAUSGARTEN Observatory. Acronyms for biogeochemical measurements performed on sediment cores are as follows: MBC (Mean bacterial Biomass per Cell), CPE (chloroplastic pigment equivalents), Lipids (phospholipid concentrations), Corg (organic carbon content), and H₂O (water content). An asterisk (*) denotes core parameters averaged (Corg and H2O) or summed (CPE, Lipids, Bacterial activities, particulate protein) over the top five centimeters of the sediment. All meiofauna abundance and biogeochemical variables included in the correlogram are described in the supplementary file. The colors corresponding to each subnetwork (Sn) are consistent across the subplots.

Fig. 5. Pelagic-benthic coupling and its partitioning according to the graph-alignment analysis of the subnetworks associated with the carbon cycle.

a Hiveplot representing both the subnetworks co-occurrence (pelagic on the two left axis: Sn_3-purple and Sn_11-blue; benthic on the two right axis: Sn_1-green) and the sequences alignment (orange edges) at alpha 0.4. The nodes on each axis are sorted by their relative abundance, their colors show the taxonomy, and their size represents the centrality of each ASV within the subnetwork 3–11 and subnetwork 1, respectively, for pelagic and benthic ecosystems. Each axis was split into two parts; the internal nodes representing the ASV sequences found in the pelagic and benthic subnetworks and the external nodes for ASV found only in the pelagic subnetworks or only in the benthic subnetwork. b Alluvial plot showing the partitioning between pelagic and benthic environments based on the alignment and the taxonomy. Line width indicates the number of ASVs aligned between the two environments, signifying connectivity between those specific phyla.