Light-Induced Energy Dissipation in Iron-Starved Cyanobacteria: Roles of OCP and IsiA Proteins

Abstract

In response to iron deficiency, cyanobacteria synthesize the iron stress–induced chlorophyll binding protein IsiA. This protein protects cyanobacterial cells against iron stress. It has been proposed that the protective role of IsiA is related to a blue light–induced nonphotochemical fluorescence quenching (NPQ) mechanism. In iron-replete cyanobacterial cell cultures, strong blue light is known to induce a mechanism that dissipates excess absorbed energy in the phycobilisome, the extramembranal antenna of cyanobacteria. In this photoprotective mechanism, the soluble Orange Carotenoid Protein (OCP) plays an essential role. Here, we demonstrate that in iron-starved cells, blue light is unable to quench fluorescence in the absence of the phycobilisomes or the OCP. By contrast, the absence of IsiA does not affect the induction of fluorescence quenching or its recovery. We conclude that in cyanobacteria grown under iron starvation conditions, the blue light–induced nonphotochemical quenching involves the phycobilisome OCP–related energy dissipation mechanism and not IsiA. IsiA, however, does seem to protect the cells from the stress generated by iron starvation, initially by increasing the size of the photosystem I antenna. Subsequently, the IsiA converts the excess energy absorbed by the phycobilisomes into heat through a mechanism different from the dynamic and reversible light-induced NPQ processes.

Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria

“…It is constitutively expressed (13), although under stress conditions (e.g., high light, salt stress, iron starvation) the levels of OCP transcripts and proteins are increased (13,18,19). Highly conserved (80-50% identity) homologues of the OCP gene are found in most PB-containing cyanobacteria (26 of 39 strains) for which genomic data are available (20).…”

“…In mutants in which the OCP was absent (12) or unable to form or stabilize the red OCP form (14, 15), blue-green light did not induce fluorescence quenching or the photoprotective mechanism. Conversely, the presence of high concentrations of OCP increases fluorescence quenching (13,14).In darkness, OCP r spontaneously reverts into the orange form and, in vivo, a recovery of the lost fluorescence is observed. However, the fluorescence recovery kinetics in vivo are slower than the OCP r -to-OCP o dark conversion in vitro, suggesting that the OCP r form is more stable in vivo than in vitro (14).…”

A photoactive carotenoid protein acting as light intensity sensor

“…The OCP appears to act as a photoreceptor, responding to blue-green light; this induces energy dissipation, resulting in a detectable quenching of the cellular fluorescence, known as nonphotochemical-quenching (NPQ), through interaction with the phycobilisome (9,11). In mutants containing the OCP but lacking phycobilisomes, blue-green light was unable to induce the photoprotective mechanism (9,10).…”

“…Only within the last few years has a photoprotective mechanism associated with the soluble phycobilisome antenna of PSII in cyanobacteria been demonstrated (8)(9)(10)(11)(12)(13)(14). A specific soluble carotenoid protein, the orange carotenoid protein (OCP), plays an essential role in this process (9,10). In its absence, thermal dissipation is abolished, rendering the cells more sensitive to high light intensities; this is manifested as a faster decrease in PSII activity in a mutant lacking the OCP (9).…”

“…In contrast, the mechanism of thermal energy dissipation in cyanobacteria, which plays a key role in global carbon cycling, remained elusive. Only within the last few years has a photoprotective mechanism associated with the soluble phycobilisome antenna of PSII in cyanobacteria been demonstrated (8)(9)(10)(11)(12)(13)(14). A specific soluble carotenoid protein, the orange carotenoid protein (OCP), plays an essential role in this process (9,10).…”