Environmental disturbances and cyanobacterial traits shape prokaryotic dynamics in a eutrophic Mediterranean coastal lagoon.

backgroundCoastal ecosystems face increasing threats from eutrophication, driven by excess nutrient inputs that lead to ecosystem-disruptive algal blooms (EDABs). The Mar Menor coastal lagoon, located in the south-eastern Iberian Peninsula, has experienced severe ecological disruption since 2015, beginning with a Synechococcus‑dominated cyanobacterial bloom and followed by major shifts in eukaryotic phytoplankton composition. However, the mechanisms that affect phytoplankton dynamics in this coastal environment remain unknown. Here, we investigate the spatiotemporal dynamics of prokaryotic communities in the lagoon after the initial Synechococcus bloom using three years of 16S rRNA gene sequencing data and evaluate how environmental factors shape these patterns. In addition, we examine the fine‑scale diversity and dynamics of Synechococcus variants through metagenomics (petB gene) and use genome‑resolved analyses to identify functional traits associated with their succession in the lagoon. Finally, to investigate the role of biotic interactions in regulating cyanobacterial growth, we examine the temporal dynamics of cyanophages.

resultsMicrobial communities in the waters of the Mar Menor responded rapidly and consistently to short‑term environmental fluctuations and showed a weak seasonal signal in alpha and beta diversity. Prokaryotic assemblages associated with two deoxygenation events following extreme weather conditions (intense rainfall in autumn 2019 and unusually high temperatures in summer 2021) illustrated how episodic disturbances can drive substantial shifts in microbial composition; notably, Synechococcus became particularly prevalent after the intense rainfall event. Fine‑scale analyses of 16S rRNA and petB gene variants revealed that a restricted set of Synechococcus lineages dominated throughout the study period. Comparative genomic analyses of these cyanobacterial populations highlighted distinct functional repertoires, including genes involved in osmoprotectant biosynthesis, diverse toxin-antitoxin systems, herbicide resistance, and multiple viral defense mechanisms, present only in specific variants. Finally, temporal analyses of viral assemblages indicated that cyanophages played a key role in modulating Synechococcus population dynamics.

conclusionsThe temporal dynamics of prokaryotic communities in the Mar Menor indicate that the lagoon remains in an altered, non‑equilibrium state, likely sustained by recurrent anthropogenic and climatic pressures. The contrasting microbial responses observed during two different deoxygenation events underscore the ecosystem's complexity. This study highlights the importance of incorporating microbial community analyses into long‑term monitoring of threatened coastal systems, and the power of comparative genomics for identifying functional traits that enable cyanobacterial proliferation in disturbed ecosystems.