Beyond blooms: A novel time series analysis framework predicts seasonal keystone species and sheds light on Arctic pelagic ecosystem stability

Abstract

A thorough understanding of ecosystem functioning in the Arctic Ocean, a region under severe threat by climate change, requires detailed studies on inhabiting biological communities. The identification of keystone species with special ecological relevance is of great importance, yet difficult to achieve with established community assessments. In the case of microbes, metabarcoding and metagenomics offer fundamental insights into community structure and function, yet remain limited regarding conclusions about the role of individual species within the ecosystem. To overcome this limitation, we have developed an analytical approach based on three different methods: Co-Occurrence Networks, Convergent Cross Mapping, and Energy Landscape Analysis. These methods enable the identification of seasonal communities in microbial ecosystems, elucidate their interactions, and predict potential stable community configurations under varying environmental conditions. Combining the outcomes of these three methods allowed us to define 19 keystone species that are representative for the different trophic modes that build the local food web. They may serve as indicator species for monitoring the consequences of environmental change in Arctic marine ecosystems. Our research reveals a clear seasonal pattern in the composition of the microbial phytoplankton community, with distinct assemblages characterizing the carbon fixation (light) and consumption (dark) phases. Species interactions exhibit strong seasonality, and we observed summer communities with significant influence on winter communities but not vice versa. During spring thaw, two distinct groups are present: consumers (heterotrophs), strongly linked to the dark phase, and photoautotrophs (mainly Bacillariophyta), initiating growth (photoautotrophic Bacillariophyta). These groups are not causally related, suggesting a "winter reset" with selective effects that facilitates a new blooming period, allowing survivors of the dark phase to emerge. Investigating the fragility of these ecological systems using Energy Landscape Analysis we demonstrate that winter communities are more stable than summer communities. In summary, the ecological landscape of the Fram Strait can be categorized by two distinct phases: a production phase governed by specialized organisms that are highly responsive to environmental changes, and a consumption phase dominated by generalist species with enhanced resilience.