Transcriptome remodeling drives acclimation to iron availability in the marine N-fixing cyanobacterium IMS101.

While enhanced phytoplankton growth as a result of iron (Fe) fertilization has been extensively characterized, our understanding of the underlying mechanisms remains incomplete. Here, we show in a laboratory setup mimicking Fe fertilization in the field that transcriptome remodeling is a primary driver of acclimation to Fe availability in the marine diazotrophic cyanobacterium IMS101. Fe supplementation promoted cell growth, photosynthesis and N fixation, and concomitant expression of the photosynthesis and N fixation genes. The expression of genes encoding major Fe-binding metalloproteins is tightly linked to cellular carbon and nitrogen metabolism and appears to be controlled by the ferric uptake regulator FurA, which is involved in regulating Fe uptake and homeostasis. This feedback loop is reinforced by substitutive expression of functionally equivalent or competitive genes depending on Fe availability, as well as co-expression of multiple Fe stress inducible genes, an adaptive strategy evolved to elicit the Fe-responsive cascade. The study provides a genome-wide perspective on the acclimation of a prominent marine diazotroph to Fe availability, reveals an upgraded portfolio of indicator genes that can be used to better assess Fe status in the environment, and predicts scenarios of how marine diazotrophs may be affected in the future ocean.IMPORTANCEThe scarcity of trace metal iron (Fe) in global oceans has a great impact on phytoplankton growth. While enhanced primary productivity as a result of Fe fertilization has been extensively characterized, the underlying molecular mechanisms remain poorly understood. By subjecting the model marine diazotroph IMS101 to increasing concentrations of supplemented Fe, we demonstrate in it a comprehensively remodeled transcriptome that drives the mobilization of cellular Fe for coordinated carbon and nitrogen metabolism and reallocation of energy and resources. Our data provide broad genomic insight into marine diazotrophs acclimation to Fe availability, enabling the versatility and flexibility in choice of indicator genes for monitoring Fe status in the environment and having implications on how marine diazotrophs persist into the future ocean.