Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: The function of IdiA and IsiA

Abstract

In this review we give an overview on the adaptational responses of photosystem (PS) II and PSI in cyanobacteria to iron starvation, mainly summarizing our results with the mesophilic Synechococcus elongatus PCC 7942. We also discuss this process with respect to the strong interrelationship between iron limitation and oxidative stress that exists in cyanobacteria as oxygenic photosynthetic organisms. The adaptation of the multiprotein complexes PSII and PSI to iron starvation is a sequential process, which is characterized by the enhanced expression of two major iron-regulated proteins, IdiA (iron deficiency induced protein A) and IsiA (iron stress induced protein A). Our results suggest that IdiA protects the acceptor side of PSII against oxidative stress under conditions of mild iron limitation in a currently unclear way, whereas prolonged iron deficiency leads to the synthesis of a chlorophyll a antenna around PSI-trimers consisting of IsiA molecules. The physiological consequences of these alterations under prolonged iron starvation, as shown by acridine yellow fluorescence measurements, are a reduction of linear electron transport activity through PSII and an increase of cyclic electron flow around PSI as well as an increase in respiratory activity. IdiA and IsiA expression are mediated by two distinct helix-turn-helix transcriptional regulators of the Crp/Fnr family. IdiB positively regulates expression of idiA under iron starvation, and Fur represses transcription of isiA under iron-sufficient conditions. Although both transcriptional regulators seem to operate independently of each other, our results indicate that a cross-talk between the signal transduction pathways exists. Moreover, IdiA as well as IsiA expression are affected by hydrogen peroxide. We suggest that due to the interdependence of iron limitation and the formation of reactive oxygen species, peroxide stress might be the superior trigger that leads to expression of these proteins under iron starvation. The modifications of PSII and PSI under iron starvation influence the redox state of redox-sensitive components of the electron transport chain, and thus the activity of metabolic pathways being regulated in dependence of the redox state of these components.

In situ transcriptomic analysis of the globally important keystone N2-fixing taxon Crocosphaera watsonii

“…isiA is formed under prolonged iron stress in cultures of cyanobacteria as a mechanism to prevent high-lightinduced oxidative damage by increasing cyclical electron flow around the photosynthetic reaction center photosystem I (Michel and Pistorius, 2004;Ohkawa et al, 2000). isiA sequences were recovered from transcriptomes at other stations in the southwest Pacific Ocean and the eastern portion of the equatorial North Atlantic Ocean (Supplementary Table 1), suggesting that this transcript may be a useful marker for the physiological status of natural populations of C. watsonii and may be more sensitive than the idiA (Webb et al, 2001), transcripts of which were not detected in our libraries.…”

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

“…However, when iron limitation in cyanobacterial cells becomes severe, excess light energy cannot be utilized by the modified or degraded PBSs, and leads to the formation of ROS and resultant oxidative stress (Latifi et al, 2009;Michel & Pistorius, 2004). Iron-limitation and oxidative stress responses in cyanobacteria are therefore closely linked (Latifi et al, 2009).…”

“…Iron-limitation and oxidative stress responses in cyanobacteria are therefore closely linked (Latifi et al, 2009). An additional contributor to increased ROS levels under iron limitation may be the reduced accumulation and/or activity of iron-dependent ROS scavengers or detoxifying enzymes (Michel & Pistorius, 2004). In our study, higher ROS production was detected in cells grown under iron-limited conditions and was higher Representative optical slices from a Z-series of DIC images (a-p) and maximum-intensity projection of PBP autofluorescence images (q-ff) of SF33 WT pigmentation strain (a-d and q-t), and DrcaE mutant (e-h and u-x), DrcaF mutant (i-l and y-bb) and DrcaC mutant (m-p and cc-ff) strains.…”

“…Based on the read counts, differential expression analysis between two treatments was calculated by DESeq (Anders & Huber, 2010). We assessed predicted annotations to identify proteins associated with responses to iron limitation, including catalases, peroxidases and SODs (Michel & Pistorius, 2004).…”

Evolved physiological responses of phytoplankton to their integrated growth environment

“…Iron was readily available in the reducing environment of early Earth and is an effective redox agent, so it was widely integrated into core electron transport components (Raven 1988(Raven , 1990Falkowski & Raven 1997). For example, a single copy of each PET component involved in linear electron transport from water to NADPH requires 24 Fe atoms (Michel & Pistorius 2004). The advent of this incredible oxygenic photosynthesis system, however, had the unfortunate side effect of altering the Earth so profoundly that it threatened not only the existence of its inventor, but all other life.…”