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

Abstract

ABSTRACTA thorough understanding of ecosystem functioning in the Arctic Ocean, a region under severe threat by climate change, requires detailed studies on linkages between biodiversity and ecosystem stability. The identification of keystone species with special relevance for ecosystem stability 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 the ecological relevance of individual taxa. 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 38 keystone species in the Arctic Fram Strait that represent different trophic modes within the food web, and might signify indicator for ecosystem functionality under the impact of environmental change. Our research reveals a clear seasonal pattern in phytoplankton composition, with distinct assemblages characterizing the phases of carbon fixation (polar day) and consumption (polar night). Species interactions exhibited strong seasonality, with significant influence of summer communities on winter communities but not vice versa. Spring harbored two distinct groups: consumers (heterotrophs), strongly linked to polar night, and photoautotrophs (mainly 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. Energy Landscape Analysis showed that winter communities are more stable than summer communities. In summary, the ecological landscape of the Fram Strait can be categorized into two distinct phases: a production phase governed by specialized organisms that are highly responsive to environmental variability, and a heterotrophic phase dominated by generalist species with enhanced resilience.