Regulation of the Distribution of Chlorophyll and Phycobilin-Absorbed Excitation Energy in Cyanobacteria. A Structure-Based Model for the Light State Transition

Abstract

The light state transition regulates the distribution of absorbed excitation energy between the two photosystems (PSs) of photosynthesis under varying environmental conditions and/or metabolic demands. In cyanobacteria, there is evidence for the redistribution of energy absorbed by both chlorophyll (Chl) and by phycobilin pigments, and proposed mechanisms differ in the relative involvement of the two pigment types. We assayed changes in the distribution of excitation energy with 77K fluorescence emission spectroscopy determined for excitation of Chl and phycobilin pigments, in both wild-type and state transition-impaired mutant strains of Synechococcus sp. PCC 7002 and Synechocystis sp. PCC 6803. Action spectra for the redistribution of both Chl and phycobilin pigments were very similar in both wild-type cyanobacteria. Both state transitionimpaired mutants showed no redistribution of phycobilin-absorbed excitation energy, but retained changes in Chl-absorbed excitation. Action spectra for the Chl-absorbed changes in excitation in the two mutants were similar to each other and to those observed in the two wild types. Our data show that the redistribution of excitation energy absorbed by Chl is independent of the redistribution of excitation energy absorbed by phycobilin pigments and that both changes are triggered by the same environmental light conditions. We present a model for the state transition in cyanobacteria based on the x-ray structures of PSII, PSI, and allophycocyanin consistent with these results.The effective absorption of sunlight by antenna pigments is the critical first step in photosynthesis. All oxygenic photosynthetic organisms share a common core antenna pigment complement of about 40 chlorophyll (Chl) a in PSII and about 100 Chl a in PSI (Rö gner et al., 1990). Photosynthetic organisms do not, however, limit their photon capturing ability to this level, but rather use some form of additional peripheral antenna pigments to increase the effective "absorption cross section" of one or both PSs. Higher plants and algae have evolved diverse mechanisms to increase their ability to absorb sunlight. In cyanobacteria, the soluble phycobiliproteins are organized into phycobilisomes (PBSs), which are primarily associated excitonically with PSII in a manner analogous to the family of intrinsic thylakoid membrane Chl a/b-containing light-harvesting complex polypeptides (LHCII), which serve the same function in higher plants (Glazer, 1984; Zilinskas and Greenwald, 1986).Both cyanobacteria and higher plants can regulate the efficiency of excitation energy transfer to the two PSs. The light state transition appears designed to adjust the relative activities of PSII and PSI in response to a dynamic environment or to changing metabolic demands (Yu et al., 1993). The mechanism in higher plants involves a reversible association of LHCII with PSII and PSI triggered by the redox state of intersystem electron transport carriers and driven by the reversible phosphorylation of LHCII (for review, see Allen, 1992; Woll...

Phycobilisome Diffusion Is Required for Light-State Transitions in Cyanobacteria

“…Phycobilisomes also diffuse more rapidly in PsaL mutants, which is consistent with the idea that state transitions involve phycobilisome mobility (Aspinwall et al, 2004). However, other models that do not involve the movement of phycobilisomes have been proposed (Schluchter et al, 1996;McConnell et al, 2002). Our current results indicate that phycobilisome mobility is critical for state transitions: the same conditions that immobilize phycobilisomes also lock cells into the light state to which they were adapted.…”

“…Recent work has led to a consensus that state transitions involve changes in the relative energy transfer from phycobilisomes to the PSI and PSII reaction centers (Mullineaux, 1994;Schluchter et al, 1996;McConnell et al, 2002). This is usually accompanied by a redistribution of chlorophyll-absorbed energy, although the two effects can be separated (Emlyn-Jones et al, 1999;McConnell et al, 2002).…”

“…Although cyanobacteria lack LHCII, they perform state transitions that are analogous to those of green plants (Fork and Satoh, 1983). State transitions in cyanobacteria involve the redistribution of phycobilisome-absorbed energy between PSII and PSI (van Thor et al, 1998;McConnell et al, 2002), and one effect of the transition to State 2 is the functional decoupling of phycobilisomes from PSII and their reassociation with PSI (Mullineaux, 1992). The biochemical mechanism is not known.…”

Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms

“…This change in gas composition decreased the standing biomass concentration, as measured by optical density at 730 nm, from 0.45 to Ϸ0.325. A color change from bluish-green to yellow corresponded with a significant increase in the chlorophyll-tophycobilin ratio (1.03 at 678:625 nm), which is consistent with a decrease in phycobilin production (19). Coincidently, cells produced extracellular appendages that linked cells into flocculated aggregates.…”

Carbon and Nitrogen Fixation byAnabaena fertilissimaunder Elevated CO2and Temperature

“…Synthesis of phycobilins is particularly susceptible to environmental influences, and there is evidence for the redistribution of energy absorbed by both chlorophyll and phycobilins under varying environmental conditions andlor metabolic demands (McConnell et al 2002). We found that production of pigments increased in A. fertilissirna at elevated C 0 2 and the enhanced photosynthesis in turn led to increases in biomass, carotenoids, and proteins.…”