Transcriptome-resolved diel metabolism of a coastal Phaeocystis bloom links cellular physiology to carbon cycling

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Abstract

Planktonic photoautotrophs drive the oceanic carbon cycle by fixing atmospheric CO₂ into organic matter, thereby regulating planetary biogeochemical fluxes. Yet, how the temporal dynamics of phytoplankton metabolism scale to ecosystem-level processes remains poorly resolved, particularly in dynamic coastal environments. In such systems, the haptophyte Phaeocystis globosa regularly forms extensive blooms, producing polysaccharide-rich gels that support colony formation and modulate carbon, nutrient, and oxygen fluxes. These blooms thus offer a natural laboratory to investigate the physiological underpinnings of coastal biogeochemistry. Here, we combine hourly metatranscriptomic profiling with photophysiological and carbonate chemistry measurements during an active P. globosa bloom in the southern North Sea. We identify diel transcriptional oscillations in metabolic pathways, with daytime gene expression enriched in photosynthesis and glycosaminoglycan biosynthesis and export, and nighttime expression linked to growth, replication, nutrient uptake, and stress response. By correlating gene expression with in situ carbon drawdown and oxygen production, we identify candidate molecular markers of primary production, including key enzymes in light harvesting and polysaccharide synthesis. Our findings demonstrate how transcriptome-resolved diel dynamics of bloom-forming phytoplankton can reveal mechanistic links between cellular physiology and ecosystem-scale carbon cycling, providing a framework to enhance molecular monitoring of coastal ocean function. *Michiel Perneel and Jens H. Dujardin contributed equally to this work.

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