A global transcriptional activator involved in the iron homeostasis in cyanobacteria.

Cyanobacteria use a series of adaptation strategies and a complicated regulatory network to maintain intracellular iron (Fe) homeostasis. Here, a global activator named IutR has been identified through three-dimensional chromosome organization and transcriptome analysis in a model cyanobacterium Synechocystis sp. PCC 6803. Inactivation of all three homologous IutR-encoding genes resulted in an impaired tolerance of Synechocystis to Fe deficiency and loss of the responses of Fe uptake-related genes to Fe-deplete conditions. Protein-promoter interaction assays confirmed the direct binding of IutR with the promoters of genes related to Fe uptake, and chromatin immunoprecipitation sequencing analysis further revealed that in addition to Fe uptake, IutR could regulate many other physiological processes involved in intracellular Fe homeostasis. These results proved that IutR is an important transcriptional activator, which is essential for cyanobacteria to induce Fe-deficiency response genes. This study provides in-depth insights into the complicated Fe-deficient signaling network and the molecular mechanism of cyanobacteria adaptation to Fe-deficient environments.

Interactions between the nitrogen-fixing cyanobacterium Trichodesmium and siderophore-producing cyanobacterium Synechococcus under iron limitation.

As diazotrophic cyanobacteria of tremendous biomass, Trichodesmium continuously provide a nitrogen source for carbon-fixing cyanobacteria and drive the generation of primary productivity in marine environments. However, ocean iron deficiencies limit growth and metabolism of Trichodesmium. Recent studies have shown the co-occurrence of Trichodesmium and siderophore-producing Synechococcus in iron-deficient oceans, but whether siderophores secreted by Synechococcus can be used by Trichodesmium to adapt to iron deficiency is not clear. We constructed a mutant Synechococcus strain unable to produce siderophores to explore this issue. Synechococcus filtrates with or without siderophores were added into a Trichodesmium microbial consortium consisting of Trichodesmium erythraeum IMS 101 as the dominant microbe with chronic iron deficiency. By analyzing the physiological phenotype, metagenome, and metatranscriptome, we investigated the interactions between the nitrogen-fixing cyanobacterium Tricodesmium and siderophore-producing cyanobacterium Synechococcus under conditions of iron deficiency. The results indicated that siderophores secreted by Synechococcus are likely to chelate with free iron in the culture medium of the Trichodesmium consortium, reducing the concentration of bioavailable iron and posing greater challenges to the absorption of iron by Trichodesmium. These findings revealed the characteristics of iron-competitive utilization between diazotrophic cyanobacteria and siderophore-producing cyanobacteria, as well as potential interactions, and provide a scientific basis for understanding the regulatory effects of nutrient limitation on marine primary productivity.

Diversity and Evolution of Iron Uptake Pathways in Marine Cyanobacteria from the Perspective of the Coastal Strain Synechococcus sp. Strain PCC 7002.

Marine cyanobacteria contribute to approximately half of the ocean primary production, and their biomass is limited by low iron (Fe) bioavailability in many regions of the open seas. The mechanisms by which marine cyanobacteria overcome Fe limitation remain unclear. In this study, multiple Fe uptake pathways have been identified in a coastal strain of Synechococcus sp. strain PCC 7002. A total of 49 mutants were obtained by gene knockout methods, and 10 mutants were found to have significantly decreased growth rates compared to the wild type (WT). The genes related to active Fe transport pathways such as TonB-dependent transporters and the synthesis and secretion of siderophores are found to be essential for the adaptation of Fe limitation in Synechococcus sp. PCC 7002. By comparing the Fe uptake pathways of this coastal strain with other open-ocean cyanobacterial strains, it can be concluded that the Fe uptake strategies from different cyanobacteria have a strong relationship with the Fe bioavailability in their habitats. The evolution and adaptation of cyanobacterial iron acquisition strategies with the change of iron environments from ancient oceans to modern oceans are discussed. This study provides new insights into the diversified strategies of marine cyanobacteria in different habitats from temporal and spatial scales. IMPORTANCE Iron (Fe) is an important limiting factor of marine primary productivity. Cyanobacteria, the oldest photosynthetic oxygen-evolving organisms on the earth, play crucial roles in marine primary productivity, especially in the oligotrophic ocean. How they overcome Fe limitation during the long-term evolution process has not been fully revealed. Fe uptake mechanisms of cyanobacteria have been partially studied in freshwater cyanobacteria but are largely unknown in marine cyanobacterial species. In this paper, the characteristics of Fe uptake mechanisms in a coastal model cyanobacterium, Synechococcus sp. PCC 7002, were studied. Furthermore, the relationship between Fe uptake strategies and Fe environments of cyanobacterial habitats has been revealed from temporal and spatial scales, which provides a good case for marine microorganisms adapting to changes in the marine environment.