Adaptation to high light intensity in Synechococcus sp. strain PCC 7942: regulation of three psbA genes and two forms of the D1 protein

Abstract

The three psbA genes in the cyanobacterium Synechococcus sp. strain PCC 7942 encode two distinct forms of the DI protein of photosystem II. ThepsbAI message, which encodes form I, dominates the psbA transcript pool at low to moderate light intensities; however, exposure to high light triggers a response in which the psbAI message is actively degraded while psbAII and psbAIII, which encode form II, are transcriptionally induced. We addressed whether these changes result from a generalized stress response and examined the consequence of light-responsive psbA regulation on the composition of DI in thylakoid membranes. Heat shock and oxidative stress had some effect on levels of the three psbA transcripts but did not produce the responses generated by an increase in light intensity. Prolonged exposure to high light (24-h time course) was characterized by elevated levels of all psbA transcripts through maintenance of high levels ofpsbAII and psbAIII messages and a rebound of the psbAI transcript after its initial decline. Form II-encoding transcripts were enriched relative to those encoding form I at all high-light time points. Form II replaced form I in the thylakoid membrane at high light despite an abundance of psbAI transcript at later time points; this may be explained by the observed faster turnover of form I than form II in the membrane. We propose that form II is less susceptible to damage at high light and that this qualitative alteration, coupled with increased turnover of Dl, protects the cells from photoinhibition.Photosystem II (PSII) is a membrane-embedded proteinpigment complex involved in key reactions of oxygenic photosynthesis: charge separation in response to excitation of a chlorophyll molecule by light and by oxygen evolution. This mode of photosynthesis, which requires two photosystems (PSII and photosystem I), is conserved in cyanobacteria, algae, and higher plants. The reaction center of PSII contains two structurally similar proteins, Dl and D2, which harbor the photoreactants involved in the primary reactions. Dl and D2, along with cytochrome b559 and the 4.8-kDapsbI gene product, form the core of the PSII reaction center (16,31,33).Light intensity modulates the composition of thylakoid membranes in plants as well as in cyanobacteria to best use the available light (2,3,30). This involves variation in the relative proportions of light-harvesting pigments, PSII and photosystem I reaction centers, electron carriers, and ATP synthase (2). On exposure to light intensities in excess of those found in optimal growth conditions, a decline in photosynthetic capacity, i.e., oxygen evolution and CO2 fixation, which is termed photoinhibition, occurs. The Dl protein is believed to be the initial site of photoinhibition, with its damage reflected in the loss of PSII activity (26,35). The DI protein of plants is rapidly turned over in the light, with the rate being proportional to light intensity. Thus, it is thought to play a role in protection of PSII against photoinhibition and may be designed to be re...

Modeling of the D1/D2 proteins and cofactors of the photosystem II reaction center: Implications for herbicide and bicarbonate binding

“…In a related cyanobacterial species, Synechococcus sp. PCC 7942, there are two distinct forms of Dl protein, one (form I, encoded by psbA-1) having a lower photochemical yield and higher susceptibility to photoinhibitory damage than the other (form 11, encoded by psbA-2 and -3) (Clarke et al, 1993;Kulkarni & Golden, 1994. The more efficient form I1 turns out to have a glutamate at 130 position, whereas the less efficient form I has a glutamine (see Svensson et al, 1991).…”

Light-responsive gene expression in cyanobacteria

“…In the laboratory, this is demonstrated by a low-to high-light shift equivalent to the increase in light intensity that a cell in shallow water might experience when a cloud moves away from blocking the sun. At low light, greater than 80% of the psbA transcripts are from psbAI, and the only D1 protein detectable in the thylakoid membrane is form I, the product of this gene (13,32). Immediately upon a shift to high light, the psbAII and psbAIII genes are induced, and the psbAI message is actively degraded (34).…”

“…Immediately upon a shift to high light, the psbAII and psbAIII genes are induced, and the psbAI message is actively degraded (34). After 30 min of exposure, the psbAII message makes up 80% of the psbA transcript population, and the identical products of this message and that of psbAIII, collectively known as form II, are substituted for form I in the thylakoid (13,32). Several lines of evidence suggest that the two forms of D1 are functionally distinct and that form II provides a selective advantage at high light (12,13,32,33).…”

Long-term microclimatic stress causes rapid adaptive radiation of kaiABC clock gene family in a cyanobacterium, Nostoc linckia , from “Evolution Canyons” I and II, Israel

“…Thus far, extensive studies have been done to ascertain molecular and genetic mechanisms of cyanobacterial responses to various stresses (see refs. [5][6][7][8][9].…”