Comparable temperatures but different microbiomes: long-term time series exposes seasonally divergent Baltic Sea prokaryotic communities

Abstract Marine microbiomes exhibit seasonal dynamics in many ocean regions. While we can characterize the biodiversity and composition of ocean microbiomes, we lack a systematic understanding of how environmental drivers shape the seasonal succession of marine microbes. To leverage the pronounced temporal changes in growth conditions in the temperate waters of the Baltic Sea, we here report on dynamics in the prokaryoplankton community over 13 years at the Linnaeus Microbial Observatory (LMO), focusing on both free-living (FL; 0.2–3 μm fraction) and particle-associated (PA; >3 μm fraction) prokaryotes. As expected, our analysis showed a higher diversity in the PA compared to the FL fraction and that the grand majority of 16S rRNA gene amplicon sequence variants (ASVs) were consistently rare. Yet, to an unexpected degree also a majority of the abundant ASVs transitioned into the rare biosphere over extended periods of the year. Prokaryotes in both the PA and FL fractions showed pronounced seasonal dynamics, with notable differences between the fractions from phylum down to the ASV level. Abundant ASVs were strongly correlated to several environmental drivers, including nutrient concentrations, salinity and temperature. Intriguingly, at comparable temperatures in spring and autumn (e.g. at 12 °C), the community composition was strikingly different. This highlighted that specific temperature values per se are informative, but that the trajectories of change in temperature and other environmental drivers (low to high, high to low) merit attention in ecological research. Our data suggest that the community composition of prokaryoplankton in temperate regions strongly depend on factors beyond temperature and photoperiod values, including the history of the community, the direction of environmental change, and qualitative and quantitative levels of (in)organic nutrients, as well as biotic interactions.