Long-Term Acclimation to Iron Limitation Reveals New Insights in Metabolism Regulation of Synechococcus sp. PCC7002

Abstract

In large areas of the ocean phytoplankton growth is limited by the scarcity of iron (Fe), an essential co-factor for multiple enzymes. Phytoplankton has hence developed strategies to survive under Fe limitation. Here, we characterize the response to Fe limitation of the cyanobacterium Synechococcus sp. PCC7002 acclimated to different Fe concentrations in chemically characterized synthetic seawater. The inorganic Fe concentrations used represent levels of Fe limitation relevant for different domains of the contemporary ocean. Combining physiological and transcriptomic approaches, we provide evidence of the progression of the physiological responses to increasing levels of Fe limitation. Our results showed a rising number of significantly regulated genes and the complexity of the response to increasing Fe limitation. Mild Fe limitation induced up-regulation of genes involved in Fe uptake, while genes involved in photosynthesis and respiration were down-regulated. Strong Fe limitation induced up-regulation of genes involved in energy metabolism and concomitant down-regulation of macronutrients uptake. Severe Fe limitation affected fine metabolic regulation of co-factors expression and activation of anti-oxidative stress responses. Our results suggest that homeostasis under long-term Fe limitation put at play dramatically different mechanisms for oxidative stress mitigation and carbon metabolism than those previously reported under Fe stress. Hence, evidence the importance of acclimation processes on the performance of cyanobacteria under Fe limitation conditions.

Towards the development of a new generation of whole‐cell bioreporters to sense iron bioavailability in oceanic systems—learning from the case ofSynechococcussp. PCC7002 iron bioreporter

“…PCC7002 under increasing severity of Fe limitation (Blanco‐Ameijeiras et al . ) have demonstrated that their expression profile did not follow a linear increase proportional to the severity of Fe limitation (Fig. b).…”

“…PCC7002 acclimated to increasing severity of Fe limitation highlighted the importance of long‐term acclimation processes and showed contrasting strategies with respect to those previously reported under sudden Fe starvation (Blanco‐Ameijeiras et al . ). In previous work from Boyanapalli et al .…”

“…PCC7002 needs only about 2 × 10 −9 mol l −1 Fe T to sustain 50% of its maximum growth rate ( K μ ) under similar environmental conditions (Blanco‐Ameijeiras et al . ). Therefore, by growing the bioreporter cells acclimated to 2 × 10 −8 mol l −1 of Fe T (which corresponds to 21·5 p Fe, where p Fe represents −log [Fe 3+ ]), which represents the higher end of Fe availability range reported in marine systems (Fig.…”

“…Under Fe limitation, cells decrease their size, decrease or replace their Fe requiring enzymes, increase the expression of Fe transporters, and activate their high‐affinity transport systems such as siderophores (Blanco‐Ameijeiras et al . ). In the presence of siderophores, Fe bioavailability is expected to be enhanced for those organisms with the specific siderophore receptors while it is expected to be decreased for those who lack the receptors, such as most of the eukaryotic phytoplankton species (Hopkinson and Morel ; Hassler et al .…”

“…Additionally, cellular stress and energetic trade‐off are important in case of nutrient limitation (Blanco‐Ameijeiras et al . ).…”