How electron tunneling and uphill excitation energy transfer support photochemistry in Halomicronema hongdechloris

Abstract Halomicronema hongdechloris, the first cyanobacterium reported to produce the red-shifted chlorophyll f (Chl f) upon acclimation to far-red light, demonstrates remarkable adaptability to diverse light conditions. The photosystem II (PS II) of this organism undergoes reversible changes in its Chl f content, with levels ranging from practically zero under white-light culture conditions to a Chl f :Chl a ratio of up to 1:8 when exposed to far-red light (FRL) in the 720–730 nm range for several days. Our ps time- and wavelength-resolved fluorescence data obtained after excitation of living H. hongdechloris cells indicate that the Soret band of a far-red (FR) chlorophyll involved in charge separation absorbs at 470 nm. At 10 K, the fluorescence decay at 715–720 nm is still fast with a time constant of 165 ps indicating an efficient electron tunneling process. However, additionally, there is efficient excitation energy transfer (EET) from 715–720 nm to 745 nm with the latter resulting from FR Chl f, which mainly functions as light-harvesting pigment upon adaptation to FRL. From there, excitation energy is efficiently transferred towards the primary donor in the reaction center of PS II with an energetic uphill EET mechanism inducing charge transfer. The fluorescence data is well explained with a secondary donor PD1 represented by a red-shifted Chl a molecule with characteristic fluorescence around 715 nm and a more red-shifted FR Chl f with fluorescence around 725 nm as primary donor at the ChlD1 or PD2 position.