Elemental allocation to molecular drivers of biogeochemistry in the Southern Ocean

Abstract

Metabolic processes underpinning ocean biogeochemistry are powered by molecular machines, proteins, that require various elements to function. Yet, the allocation of elements to these proteins, and subsequent implications for biogeochemical processes, remain poorly characterized. Here we integrate elemental measurements with metaproteomics to quantitatively examine elemental use in Southern Ocean microbial proteins and metabolic processes. We demonstrate that iron availability influences elemental allocation, including decreased iron allocation to photosynthesis and compensatory incorporation of non-iron metals into metalloproteins under iron scarcity. Manganese was primarily allocated to photosynthesis in iron-replete conditions, and reallocated to other metabolic roles under low iron. Photosystem I:II protein mass ratios impacted both iron and manganese allocation, and appeared to be driven by iron availability. Approximately half of biogenic copper was found in plastocyanin, likely substituting for iron-containing cytochromes in photosynthesis. Moreover, biogenic nitrogen to phosphorus ratios were decoupled from ribosomal abundance, contrary to prevailing assumptions about ribosomal influence on stoichiometric regulation in the ocean. Instead, our results suggest that community composition and intracellular storage are important regulators of N:P in the Southern Ocean. Together, our findings identify key molecular mechanisms that modulate elemental demand and limitation, and provide a foundation for quantitatively connecting molecular measurements with biogeochemical models.