The Thermodynamics and Kinetics of Electron Transfer between Cytochrome b6f and Photosystem I in the Chlorophyll d-dominated Cyanobacterium, Acaryochloris marina

Abstract

We have investigated the photosynthetic properties of Acaryochloris marina, a cyanobacterium distinguished by having a high level of chlorophyll d, which has its absorption bands shifted to the red when compared with chlorophyll a. Despite this unusual pigment content, the overall rate and thermodynamics of the photosynthetic electron flow are similar to those of chlorophyll a-containing species. The midpoint potential of both cytochrome f and the primary electron donor of photosystem I (P 740 ) were found to be unchanged with respect to those prevailing in organisms having chlorophyll a, being 345 and 425 mV, respectively. Thus, contrary to previous reports (Hu, Q., Miyashita, H., Iwasaki, I. I., Kurano, N., Miyachi, S., Iwaki, M., and Itoh, S. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 13319 -13323), the midpoint potential of the electron donor P 740 has not been tuned to compensate for the decrease in excitonic energy in A. marina and to maintain the reducing power of photosystem I. We argue that this is a weaker constraint on the engineering of the oxygenic photosynthetic electron transfer chain than preserving the driving force for plastoquinol oxidation by P 740 , via the cytochrome b 6 f complex. We further show that there is no restriction in the diffusion of the soluble electron carrier between cytochrome b 6 f and photosystem I in A. marina, at variance with plants. This difference probably reflects the simplified ultrastructure of the thylakoids of this organism, where no segregation into grana and stroma lamellae is observed. Nevertheless, chlorophyll fluorescence measurements suggest that there is energy transfer between adjacent photosystem II complexes but not from photosystem II to photosystem I, indicating spatial separation between the two photosystems.Acaryochloris marina is an unusual cyanobacterium, because it contains mainly chlorophyll (Chl) 3 d. It was first isolated from a suspension of algae squeezed out of Lissoclinum patella, a colonial ascidian (1). It mainly grows as a biofilm on the undersurface of the ascidian beneath a symbiotic layer of a Prochloron, which is in the upper tunic of the ascidian (2). Other varieties of Acaryochloris have been found on the underside of the thallus of red algae (3) and free living in a salt lake (4). The general feature of its habitat is that it lives at relatively low light intensities, which are enriched in the far red region of the spectrum. Therefore, its oxygenic photosynthesis provides a typical example of adaptation to specific light conditions (2), as evidenced by its pigment composition, where Chl d is predominant and the Chl a level is very low (5, 6). This pigment composition contrasts with the usual high level of Chl a found in other oxygenic phototrophes, as illustrated by the absorption spectrum of a suspension of A. marina cells, which is markedly red-shifted when compared with other Chl a-containing photosynthetic organisms. The extent of the red shift of the absorption spectrum of A. marina is of similar magnitude to that observed b...

Plastid thylakoid architecture optimizes photosynthesis in diatoms

“…To assess the existence of restricted diffusion domains, we compared the theoretical equilibrium constant ( K th ) between PSI and its electron donors (cyt) with the experimental one ( K exp ), following previous approaches in plants3 and bacteria38. In P. tricornutum we calculate a value of 16 for K th , based on the redox potentials of cyt c 6 (349 mV)16 and of P 700 (420 mV)17.…”

Photosynthesis at the far-red region of the spectrum in Acaryochloris marina

“…Initially it was discovered that the redox mid-point potential ( E m ) of P 740 is 335 mV, which is 120–150 mV more negative than P 700 , which has E m  = +420 to +450 mV [2]. However later on it was found that A. marina P 740 of PSI has same redox potential like P 700 of normal PSI [36, 37]. Due to the presence of Chl d , it can absorb energy at longer wavelength than P 700 .…”

“…The midpoint potential for cytochrome f and the primary electron donor of PSI (P 740 ) were discovered to be unaltered as compare to other photosynthetic species having Chl a and it was 345 mV for Cyt- f and 425 mV for P 740 . These results revealed that the midpoint potential of the special pair is not adjusted to the incoming flux of weak excitionic energy in this organism and to conserve the reducing power of PSI [37]. Further investigations revealed that there is no hindrance in the circulation of soluble electron transport protein between cytochrome- b6f and PSI in A. marina .…”

“…The chlorophyll fluorescence measurements presented that there is an energy transfer between neighboring PSII complexes but not from PSII to PSI or vice versa. This indicated that there are empty spaces between PSII and PSI [37]. …”

“…In A. marina MBIC11017 strain the amount of phycobiliproteins is low as compared to the Awaji-1 strain and due to this reason their fluorescence properties are different, while on the other hand CCMEE5410 strain is devoid of phycobiliproteins [60, 61]. The Cryo-electron transmission microscopy images of whole cell parts showed a number of spots of near crystalline phycobiliprotein at the stromal side of the membrane [30, 37]. These patches of phycobiliproteins separate the reaction centers of the two photosystems from one another [30].…”