Exploring the phycosphere of Emiliania huxleyi: from bloom dynamics to microbiome assembly experiments

Coccolithophores have global ecological and biogeochemical significance as the most important calcifying marine phytoplankton group. The structure and selection of prokaryotic communities associated with the most abundant coccolithophore and bloom-forming species, Emiliania huxleyi, are still poorly known. In this study, we assessed the diversity of bacterial communities associated with an E. huxleyi bloom in the Celtic Sea, exposed axenic E. huxleyi cultures to prokaryotic communities derived from bloom and non-bloom conditions and followed the dynamics of their microbiome composition over one year. Bloom-associated prokaryotic communities were dominated by SAR11, Marine group II Euryarchaeota, Rhodobacterales and contained substantial proportions of known indicators of phytoplankton bloom demises such as Flavobacteriaceae and Pseudoalteromonadaceae. Taxonomic richness of replicated co-cultures resulting from natural communities with axenic E. huxleyi rapidly shifted and then stabilized over time, presumably by ecological selection favoring more beneficial populations. Recruited microbiomes from the environment were consistently dependent on the composition of the initial bacterioplankton community. Phycosphere-associated communities derived from the E. huxleyi bloom depth were highly similar to one another, suggesting deterministic processes, whereas cultures from non-bloom conditions show an effect of both deterministic processes and stochasticity. Overall, this work sheds new light on the importance of the initial inoculum composition in microbiome recruitment and elucidates the temporal dynamics of its composition and long-term stability.