Iron Deficiency in Cyanobacteria Causes Monomerization of Photosystem I Trimers and Reduces the Capacity for State Transitions and the Effective Absorption Cross Section of Photosystem I in Vivo

Abstract

The induction of the isiA (CP43#) protein in iron-stressed cyanobacteria is accompanied by the formation of a ring of 18 CP43# proteins around the photosystem I (PSI) trimer and is thought to increase the absorption cross section of PSI within the CP43#-PSI supercomplex. In contrast to these in vitro studies, our in vivo measurements failed to demonstrate any increase of the PSI absorption cross section in two strains (Synechococcus sp. PCC 7942 and Synechocystis sp. PCC 6803) of iron-stressed cells. We report that iron-stressed cells exhibited a reduced capacity for state transitions and limited dark reduction of the plastoquinone pool, which accounts for the increase in PSII-related 685 nm chlorophyll fluorescence under iron deficiency. This was accompanied by lower abundance of the NADP-dehydrogenase complex and the PSI-associated subunit PsaL, as well as a reduced amount of phosphatidylglycerol. Nondenaturating polyacrylamide gel electrophoresis separation of the chlorophyllprotein complexes indicated that the monomeric form of PSI is favored over the trimeric form of PSI under iron stress. Thus, we demonstrate that the induction of CP43# does not increase the PSI functional absorption cross section of whole cells in vivo, but rather, induces monomerization of PSI trimers and reduces the capacity for state transitions. We discuss the role of CP43# as an effective energy quencher to photoprotect PSII and PSI under unfavorable environmental conditions in cyanobacteria in vivo.

Transcript Profiling Reveals New Insights into the Acclimation of the Mesophilic Fresh-Water CyanobacteriumSynechococcus elongatusPCC 7942 to Iron Starvation

“…This result indicates that prolonged Fe limitation results in a reduction of PSI reaction center proteins and in a decreased percentage of trimerized PSI relative to the total pool of PSI. The latter finding supports previous results showing that monomeric PSI is favored over trimeric PSI in S. elongatus PCC 7942 during Fe-deficient growth conditions (Ivanov et al, 2006). A similar result was also obtained from Synechocystis sp.…”

“…In addition, IsiA has been suggested to act as a chlorophyll (Chl) sink (Burnap et al, 1993) to prevent high quantities of unbound potentially hazardous 3 Chl. IsiA also protects PSII and PSI against the damage caused by excessive light through a nonradiative type of energy dissipation (Ivanov et al, 2000(Ivanov et al, , 2006Sandströ m et al, 2001Sandströ m et al, , 2002Ihalainen et al, 2005). Besides its expression under low Fe concentrations and during conditions of oxidative stress (Jeanjean et al, 2003;Yousef et al, 2003;Li et al, 2004;Michel and Pistorius, 2004;Singh et al, 2004), IsiA is also expressed in high amounts during sodium chloride stress (Vinnemeier et al, 1998;Havaux et al, 2005), heat stress (Fulda et al, 2006), and during the stationary growth phase (Singh and Sherman, 2006).…”

Characterization and Evolution of Tetrameric Photosystem I from the Thermophilic Cyanobacterium Chroococcidiopsis sp TS-821

“…In contrast to the disadvantage of having a monomeric PSI, the psaL mutants of Synechocystis and Synechococcus showed faster growth rates than wild-type cells when DCMU was added with Glc supplement (Chitnis et al, 1993;Schluchter et al, 1996). These results indicate that having a monomeric PSI is somewhat of an advantage, which is supported by the later observation that both Synechocystis and Synechococcus downregulate the expression level of PsaL and make more monomeric PSI lacking PsaL under iron deficiency stress (Ivanov et al, 2006). In summary, PSI monomer is favored when cyanobacteria deal with stresses, possibly including high-light intensity.…”

The role of the orange carotenoid protein and PsbU protein in photoprotection in cyanobacteria

“…Since the NAD(P)H dehydrogenase is one of the most iron-abundant complexes within the cyanobacterial thylakoid membranes, its down-regulation would result in a minimal contribution of stromal reductants to the intersystem electron flow in iron-stressed cells. This would minimize dark reduction of the PQ pool and maintain iron-stressed cells in State 1 (Ivanov et al, 2006). However, this cannot explain why orange illumination failed to induce State 2 in 2 iron-starved cells.…”

“…It was also proposed that the balance between the monomeric and trimeric forms of PSI plays a role in the regulation of state transitions (Schluchter et al, 1996), with more PSI trimers in State 2 than in State 1. While in normal growth conditions the trimeric form of PSI is predominant, there is a dramatic shift to the monomeric form in iron stress conditions (Sandstrom et al, 2002;Ivanov et al, 2006) that may favor State 1. Before moving to the next step of the characterization of iron-starved cells that differ in their OCP configuration, it is worth mentioning that after these interesting results it was decided to monitor a few other cyanobacteria species that had or lacked the OCP gene.…”