Atlantic water influx and sea-ice cover drive taxonomic and functional shifts in Arctic marine bacterial communities

Abstract

The Arctic Ocean is experiencing unprecedented changes because of climate warming, necessitating detailed analyses on the ecology and dynamics of biological communities to understand current and future ecosystem shifts. Here, we generated a four-year, high-resolution amplicon dataset along with one annual cycle of PacBio HiFi read metagenomes from the East Greenland Current (EGC), and combined this with datasets spanning different spatiotemporal scales (Tara Arctic and MOSAiC) to assess the impact of Atlantic water influx and sea-ice cover on bacterial communities in the Arctic Ocean. Densely ice-covered polar waters harboured a temporally stable, resident microbiome. Atlantic water influx and reduced sea-ice cover resulted in the dominance of seasonally fluctuating populations, resembling a process of “replacement” through advection, mixing and environmental sorting. We identified bacterial signature populations of distinct environmental regimes, including polar night and high-ice cover, and assessed their ecological roles. Dynamics of signature populations were consistent across the wider Arctic; e.g. those associated with dense ice cover and winter in the EGC were abundant in the central Arctic Ocean in winter. Population- and community-level analyses revealed metabolic distinctions between bacteria affiliated with Arctic and Atlantic conditions; the former with increased potential to use bacterial- and terrestrial-derived substrates or inorganic compounds. Our evidence on bacterial dynamics over spatiotemporal scales provides novel insights into Arctic ecology and indicates a progressing Biological Atlantification of the warming Arctic Ocean, with consequences for food webs and biogeochemical cycles.

The Arctic summer microbiome across Fram Strait: Depth, longitude, and substrate concentrations structure microbial diversity in the euphotic zone

“…On average, ASVs from signature populations constituted a relative abundance of 66%, with a maximum of 78% in the lower-photic western Strait (Table S2). The maximum in subsurface Arctic waters supports the notion of a stable community in "true" polar conditions, which might be affected by progressing Atlantification (Priest, von Appen, et al, 2023). Each cluster displayed a specific taxonomic composition (Figure 7B).…”

“…Subsurface MAGs shared several CAZymes not found in surface MAGs (Figure 8A), including GH88 (chitosan or gellan hydrolase) and PL1 (pectate lyase). Most subsurface CAZymes were found in the verrucomicrobial Arctic97B‐4 clade, harbouring 81 CAZyme and 54 sulfatase genes potentially targeting semi‐refractory polysaccharides (Priest, von Appen, et al, 2023).…”

“…This cluster of 189 ASVs (Table S2) is associated with subsurface Atlantic conditions. Accordingly, the Arctic97B‐4 clade has been reported in subsurface waters (Pajares, 2021), with a particle‐associated, chemomixotrophic lifestyle (Milici et al, 2017; Priest, von Appen, et al, 2023). Little is known about Arenicella ; reported in sea‐ice‐associated microbiomes (Garneau et al, 2016) and putatively involved in nitrate reduction (Weigel et al, 2022).…”

“…Raw fastq files have been deposited at ENA under BioProject PRJEB66267. For functional predictions, ASVs were mapped to 16S rRNA gene sequences of metagenome‐assembled genomes (MAGs) from Fram Strait (Priest et al, 2021; Priest, von Appen, et al, 2023) through competitive read recruitment using BBMap in BBtools v35.14, with an identity threshold of 100% (Table S2).…”

“…Bacterial cell numbers are an order of magnitude higher in the eastern Fram Strait, which has been attributed to higher water temperatures (Cardozo‐Mino et al, 2021). Overall, Atlantic‐influenced waters are more productive and characterized by stronger seasonal dynamics (Wietz et al, 2021), with major implications for the biological carbon pump (Fadeev, Rogge, et al, 2021; Flores et al, 2019; Priest, von Appen, et al, 2023; Ramondenc et al, 2022; Rapp et al, 2018; von Appen et al, 2021). In addition to regional differences, bacterial communities in the Fram Strait distinctly vary with depth.…”