New insights into the function of the iron deficiency-induced protein C from Synechococcus elongatus PCC 7942

Abstract

Iron limitation has a strong impact on electron transport reactions of the unicellular fresh water cyanobacterium Synechococcus elongatus PCC 7942 (thereafter referred to as S. elongatus). Among the various adaptational processes on different cellular levels, iron limitation induces a strongly enhanced expression of IdiC (iron-deficiency-induced protein C). In this article, we show that IdiC is loosely attached to the thylakoid and to the cytoplasmic membranes and that its expression is enhanced during conditions of iron starvation and during the late growth phase. The intracellular IdiC level was even more increased when additional iron was replenished in the late growth phase. On the basis of its amino acid sequence and of its absorbance spectrum, IdiC can be classified as a member of the family of thioredoxin (TRX)-like (2Fe-2S) ferredoxins. The presence of an iron cofactor in IdiC was detected by inductive coupled plasma optical emission spectrometry (ICP-OES). Comparative measurements of electron transport activities of S. elongatus wild type (WT) and an IdiC-merodiploid mutant called MuD, which contained a strongly reduced IdiC content under iron-sufficient as well as iron-deficient growth conditions, were performed. The results revealed that MuD had a strongly increased light sensitivity, especially under iron limitation. The measurements of photosystem II (PS II)-mediated electron transport rates in WT and MuD strain showed that PS II activity was significantly lower in MuD than in the WT strain. Moreover, P(700) (+) re-reduction rates provided evidence that the respiratory activities, which were very low in the MuD strain in the presence of iron, significantly increased in iron-starved cells. Thus, an increase in respiration may compensate for the drastic decrease of photosynthetic electron transport activity in MuD grown under iron starvation. Based on the similarity of the S. elongatus IdiC to the NuoE subunit of the NDH-1 complex in Escherichia coli, it is likely that IdiC has a function in the electron transport processes from NAD(P)H to the plastoquinone pool. This is in agreement with the up-regulation of IdiC in the late growth phase as well as under stress conditions when PS II is damaged. As absence or high reduction of the IdiC level would prevent or reduce the formation of functional NDH-1 complexes, under such conditions electron transport routes via alternative substrate dehydrogenases, donating electrons to the plastoquinone pool, can be assumed to be up-regulated.

Methyl viologen responsive proteome dynamics ofAnabaenasp. strain PCC7120

“…NTR, exclusively found in photosynthetic organisms, is involved in chloroplast redox homeostasis by maintaining a pool of reduced thioredoxins (Trx) that, in turn, reduce intramolecular disulfide bridges in the proteins damaged by oxidative stress . Upregulated expression of Trx proteins has been reported in response to several abiotic stresses in different cyanobacteria . NTR–Trx system catalyzes regeneration of reduced 2‐Cys Prx that, in turn, detoxify hydrogen peroxide, organic peroxides, or peroxynitrite, respectively .…”

Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501

“…Furthermore, functional nitrogenase enzymes contain a high quantity of iron cofactors (in total 38 Fe atoms per nitrogenase complex) (Rubio and Ludden, ), and thus it has been argued that iron is supplied by the degradation of iron‐rich PSI complexes (36 Fe per monomeric PSI) in C. watsonii (Saito et al ., ), similarly like shown in Trichodesmium IMS101 (Shi et al ., ). Such iron recycling is well documented in cyanobacteria like Synechococcus elongatus PCC7942 where photosynthetic protein complexes are degraded in the order of PSII, PSI, and cytochrome b 6 f under iron deficiency, which prolongs survival by maintaining electron transport and energy transduction under iron stress (Pietsch et al ., ). Thus, the diel cycle of PSI in C. watsonii could be evolutionarily related to iron limitation in its natural habitat.…”

The Challenge of Iron Stress in Cyanobacteria

“…Even though IdiC synthesis is constitutive, iron limitation induces a strongly enhanced expression of idiC. IdiC is loosely attached to the thylakoid and to other membranes, and its expression is enhanced during conditions of iron starvation or during the late growth phase [57]. Even though its role is still unclear, based on the similarity of IdiC to NuoE of the respiratory Escherichia coli NDH-1 complex, it has been suggested that IdiC is a component of the NADH-1 complex in Synechococcus elongatus and, thus, has a function in the electron donation from NAD(P)H to plastoquinone.…”

“…Even though its role is still unclear, based on the similarity of IdiC to NuoE of the respiratory Escherichia coli NDH-1 complex, it has been suggested that IdiC is a component of the NADH-1 complex in Synechococcus elongatus and, thus, has a function in the electron donation from NAD(P)H to plastoquinone. Under stress conditions, when PSII resulted damaged, IdiC would prevent or reduce the oxidative stress deviating electron transport via alternative dehydrogenases, increasing PSI cyclic flow interconnected with respiratory routes [57].…”