Molybdenum isotopic fractionation during assimilation by unicellular cyanobacteria Synechococcus elongatus FACHB-1061

Abstract

Molybdenum is essential for life, but the low Mo concentration in paleo-oceans restricted its bioavailability, especially for cyanobacteria, which contributed oxygen and organic compounds to the paleo-oceans. However, the Mo assimilation mechanism of cyanobacteria and the response to different ambient Mo concentrations remain unclear. Molybdenum isotopic fractionation is sensitive to changes in the bonding environment and thus was used to investigate Mo assimilation processes in cyanobacteria. In this study, we measured the Mo isotopic compositions of Synechococcus elongatus grown in media with different Mo concentrations. Results show that at low Mo concentrations (30 nmol/L − 1500 nmol/L), Synechococcus elongatus exhibits a significantly lighter Mo isotopic composition relative to solution during the rapid growth phase (mean Δ98Mocell-medium = −2.20 ± 0.25 ‰), which gradually rises to a heavier equilibrium value (mean Δ98Mocell-medium = −1.30 ± 0.32 ‰) during the stationary phase. In contrast, at high Mo concentrations (e.g., 10000 nmol/L), the Mo isotopic composition is significantly heavier than that at low concentration (Δ98Mocell-medium = −1.13 ± 0.13 ‰) during the rapid growth phase and decreases to a lighter equilibrium value (Δ98Mocell-medium = −1.57 ± 0.16 ‰) during the stationary phase. The results suggest the coexistence of two distinct Mo transport systems in Synechococcus elongatus. Most of the Mo is assimilated by Synechococcus elongatus via the ModABC transport system, resulting in significant kinetic isotopic fractionation during transmembrane transport during the rapid growth phase. When ambient Mo concentration increases, low-affinity Mo transport systems are activated, reducing this kinetic fractionation. However, as the cyanobacteria grow, transmembrane transport reaches equilibrium under all ambient Mo concentrations during the stationary phase, where the Mo isotopic fractionation is controlled by the synthesis of Mo-containing enzymes. This study reveals that cyanobacteria dynamically adapt their Mo uptake pathways to varying Mo concentration conditions, exhibiting distinct isotopic fractionation patterns. The findings provide new insights into early microbial metal utilization and a potential isotopic tool for reconstructing paleo-ocean biogeochemistry.