Pan-proteome regulation of marine Synechococcus nutrient stress plasticity

ABSTRACT Variable phytoplankton resource demands can buffer productivity to climate-driven declines in nutrient supply, but the extent of this buffering depends on limits to cellular elemental plasticity. Elemental plasticity is driven by a combination of genomic adaptation and physiological regulation, but their mechanistic links remain unresolved. Here, we combine continuous culture experiments with proteomics and elemental analyses to determine how genomic diversity shapes nutrient stress plasticity in six strains of the globally distributed cyanobacterium Synechococcus . By maintaining fixed growth rates in chemostats under nitrogen- or phosphorus-limiting conditions, we disentangle lineage-specific resource demands from growth effects. All strains show conserved induction of nutrient acquisition pathways, yet strain identity explains most pan-proteome variance, and variation in non-core protein expression predicts deviations in elemental plasticity. Strains from oligotrophic compared to mesotrophic regions exhibit broader proteomic adjustments and wider C:P and N:P ranges. Our findings show that genomic diversity expressed through pan-proteome regulation amplifies physiological plasticity and increases phytoplankton nutrient stress buffering capacity under future climate conditions. IMPORTANCE Marine cyanobacteria are among the most abundant microbes on Earth and play central roles in global nutrient cycling, yet the molecular mechanisms that determine how they respond to nutrient stress remain poorly understood. Here, we show that genomic diversity within the marine cyanobacterium Synechococcus translates into differences in protein expression and cellular resource allocation. Combining chemostat experiments and proteomics across multiple strains, we demonstrate that variation in the non-core genome shapes how lineages regulate nutrient acquisition pathways and adjust cellular C:N:P stoichiometry under nitrogen or phosphorus stress. These results reveal how pan-genome diversity generates physiological plasticity within microbial populations, providing a mechanistic link between microbial genomic variation and ecosystem-level nutrient cycling in the ocean.