Long-term Iron and Phosphorus Co-limitation Fundamentally Restructures Protein Biochemistry of High CO2-adapted Trichodesmium

Because the globally-distributed diazotrophic cyanobacterium Trichodesmium is a critical new-nitrogen source to nutrient-deplete marine ecosystems, it is crucial to understand its evolutionary responses to global-change factors as they interact with other important environmental controls such as iron and phosphorus limitation. We grew Trichodesmium under multiple iron and phosphorus (co)-limitation scenarios for 1 year following ~7 years of adaptation to both present (380-ppm) and future (750-ppm) CO₂ concentrations, and discovered a complex metabolic response specific to Fe/P co-limitation, which includes increased growth rates, whole-cell biochemical restructuring, and cell biomass reduction. The interaction of increasing CO₂ with this nutrient co-limited state induced an additional set of comprehensive metabolic shifts away from those seen under present day CO₂, characterized by upregulation of a new complement of proteins involved in broad cellular functions, core metabolism, and growth. This restructuring reveals a unique co-limited phenotype under Fe/P “balancing” co-limitation, which fundamentally alters traditional interpretations of interactive nutrient limitations and their subsequent controls on key global biogeochemical processes in both the present and future ocean.