Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome

Deciphering how microbial communities are shaped by environmental variability is fundamental for understanding the structure and function of ocean ecosystems. Thus far, we know little about the structuring of community functionality and the coupling between taxonomy and function over seasonal environmental gradients. To address this, we employed autonomous sampling devices and in situ sensors to investigate the taxonomic and functional dynamics of a pelagic Arctic Ocean microbiome over a four-year period. We demonstrate that the dominant prokaryotic and microeukaryotic populations exhibit recurrent, unimodal fluctuations each year, with community gene content following the same trend. The recurrent dynamics within the prokaryotic microbiome are structured into five temporal modules that represent distinct ecological states, characterised by unique taxonomic and metabolic signatures and connections to specific microeukaryotic populations and oceanographic conditions. For instance, Cand. Nitrosopumilus and the machinery to oxidise ammonia and reduce nitrite are signatures of early polar night, along with Radiolarians. In contrast, late summer is characterised by Amylibacter, sulfur compound metabolism and diverse Haptophyta lineages. Exploring the composition of modules further along with their degree of functional redundancy and the structuring of genetic diversity within functions over time revealed seasonal heterogeneity in environmental selection processes. In particular, we observe strong selection pressure on a functional level in spring while late polar night features weaker selection pressure that likely acts on an organismal level. By integrating taxonomic, functional, and environmental information, our study provides fundamental insights into how microbiomes are structured under pronounced environmental variability in understudied, yet rapidly changing polar marine ecosystems.