Critical Roles of Bacterioferritins in Iron Storage and Proliferation of Cyanobacteria  

Abstract

Cyanobacteria are key contributors to global photosynthetic productivity, and iron availability is essential for cyanobacterial proliferation. While iron is abundant in the earth's crust, its unique chemical properties render it a limiting factor for photoautotrophic growth. As compared to other nonphotosynthetic organisms, oxygenic photosynthetic organisms such as cyanobacteria, algae, and green plants need large amounts of iron to maintain functional PSI complexes in their photosynthetic apparatus. Ferritins and bacterioferritins are ubiquitously present iron-storage proteins. We have found that in the cyanobacterium Synechocystis sp. PCC 6803 (Synechocystis 6803), bacterioferritins are responsible for the storage of as much as 50% of cellular iron. Synechocystis 6803, as well as many other cyanobacterial species, have two bacterioferritins, BfrA and BfrB, in which either the heme binding or di-iron center ligating residues are absent. Purified bacterioferritin complex from Synechocystis 6803 has both BfrA and BfrB proteins. Targeted mutagenesis of each of the two bacterioferritin genes resulted in poor growth under iron-deprived conditions. Inactivation of both genes did not result in a more severe phenotype. These results support the presence of a heteromultimeric structure of Synechocystis bacterioferritin, in which one subunit ligates a diiron center while the other accommodates heme binding. Notably, the reduced internal iron concentrations in the mutant cells resulted in a lower content of PSI. In addition, they triggered iron starvation responses even in the presence of normal levels of external iron, thus demonstrating a central role of bacterioferritins in iron homeostasis in these photosynthetic organisms.Iron serves as a cofactor in a multitude of cellular processes. As such, iron accumulation and storage processes are essential for the survival of all organisms. However, the same redox properties that make iron a valuable cofactor also lead to oxidative interactions resulting in the formation of harmful radicals. Therefore, iron accumulation in the cells is tightly regulated to ensure that very little free iron is present (Kakhlon and Cabantchik, 2002).While iron is abundant in the earth's crust, the bioavailability of iron in the current oxidative terrestrial environment is limited. This is due to the fact that in the presence of dioxygen at neutral pH, iron precipitates as Fe(OH) 3 . As a consequence, the bioavailability of iron limits the proliferation of photosynthetic organisms. Indeed, studies conducted in the Southern Ocean have indicated that iron is a limiting factor for primary photosynthetic productivity (Falkowski et al., 1998). In many of the ecological niches occupied by photosynthetic organisms, iron concentrations are limited to nanomolar levels (Morel and Price, 2003). Surges in the iron concentration due to aeolian dust deposition are transient (Falkowski et al., 1998). To accommodate such an infrequent supply of iron, photosynthetic organisms must have efficient iron storage mec...

Ferritin is required for rapid remodeling of the photosynthetic apparatus and minimizes photo‐oxidative stress in response to iron availability in Chlamydomonas reinhardtii

“…Despite the clear reduction of ferritin, the PSI level (Figure 5a) and the iron content per protein (Table 1) remained unchanged in the mutant. A stronger phenotype was seen in bacterioferritin knock-out strains of Synechocystis that led to a reduction of the iron content to 70% and reduction of PSI to 75% of the wild-type level under iron-sufficient conditions (Keren et al, 2004). It appears that the remaining 25% of ferritin are sufficient to sustain normal iron metabolism under iron-sufficient conditions in Chlamydomonas.…”

Metal Homeostasis in Cyanobacteria and Chloroplasts. Balancing Benefits and Risks to the Photosynthetic Apparatus

“…PCC 6803 is 2 orders of magnitude higher than that of the nonoxygenic purple bacterium Rhodobacter capsulatus (Keren et al, 2002). The Fe quota of Synechocystis cells is 1 order of magnitude higher than that of the nonphotosynthetic bacterium Escherichia coli (Keren et al, 2004). Furthermore, more than 25% of the Fe quota in Synechocystis cells is in PSI alone (Keren et al, 2004).…”

“…The Fe quota of Synechocystis cells is 1 order of magnitude higher than that of the nonphotosynthetic bacterium Escherichia coli (Keren et al, 2004). Furthermore, more than 25% of the Fe quota in Synechocystis cells is in PSI alone (Keren et al, 2004). In plant leaves, 60% to 80% of cellular Fe content is in chloroplasts (Terry and Low, 1982).…”

Responses to iron limitation are impacted by light quality and regulated by RcaE in the chromatically acclimating cyanobacterium Fremyella diplosiphon

“…Ferritin-like proteins have roles in iron storage (Keren et al, 2004), as well as organismal responses to oxidative stress in cyanobacteria (Ekman et al, 2014). We thus assessed the impact of iron limitation on a number of ferritins that we annotated in the RNa-Seq data.…”