Photochemistry beyond the red limit in chlorophyll f–containing photosystems

Abstract

Photosystems I and II convert solar energy into the chemical energy that powers life. Chlorophyll a photochemistry, using red light (680 to 700 nm), is near universal and is considered to define the energy "red limit" of oxygenic photosynthesis. We present biophysical studies on the photosystems from a cyanobacterium grown in far-red light (750 nm). The few long-wavelength chlorophylls present are well resolved from each other and from the majority pigment, chlorophyll a. Charge separation in photosystem I and II uses chlorophyll f at 745 nm and chlorophyll f (or d) at 727 nm, respectively. Each photosystem has a few even longer-wavelength chlorophylls f that collect light and pass excitation energy uphill to the photochemically active pigments. These photosystems function beyond the red limit using far-red pigments in only a few key positions.

Early Archean origin of Photosystem II

“…Several types of D1 can be distinguished phylogenetically (Cardona, Murray, & Rutherford, 2015) and their evolution is schematized in Figure 1c. The early evolving forms, referred to as atypical D1 forms (G0, G1, G2 in Figure 1), are characterized by the absence of some, but not all, of the ligands to the Mn 4 CaO 5 cluster and have been recently found to be involved in the synthesis of chlorophyll f, which supports oxygenic photosynthesis using low energy far-red light (Ho, Shen, Canniffe, Zhao, & Bryant, 2016;Nurnberg et al, 2018); or the inactivation of PSII when anaerobic processes are being carried out (Murray, 2012;Wegener, Nagarajan, & Pakrasi, 2015). The late evolving forms, referred to as the standard D1 forms, are characterized by a complete set of ligands to the Mn 4 CaO 5 cluster and are the main D1 used for water oxidation.…”

Life in the dark: far‐red absorbing cyanobacteria extend photic zones deep into terrestrial caves

“…Due to the potential of both Chl d and f to expand the usable spectrum for oxygenic photosynthesis (Chen and Blankenship, 2011), research efforts on cyanobacteria with red-shifted chlorophylls have largely focused on the investigation of their biophysical and photobiological properties (Allakhverdiev et al, 2016) and the genetic regulation of photoacclimatory responses (Gan et al, 2014b). Chl f was found to act as primary electron donors in both photosystems II and I and as linker pigments connecting to shorter wavelength antenna pigments (Nürnberg et al, 2018). Foundational work by Bryant et al has shown that many cyanobacteria can remodel their photosynthetic pigmentation under far-red light via synthesis of Chl f, Chl d and red-shifted phycobilins (Gan et al, 2014b).…”

An investigation into the effects of increasing salinity on photosynthesis in freshwater unicellular cyanobacteria during the late Archaean

“…Other strategies to overcome UV exposure would have been to grow in shaded areas under rocks (Nürnberg et al, 2018), in caves (Saw et al, 2013) or benthically Homann et al, 2016). Salt tolerance would have been necessary for oxygenic phototrophs living in marine and brackish environments (Blank, 2013).…”

“…Based on these studies, C. thermalis PCC7203 has been proposed as an early Earth terrestrial coloniser (Billi et al, 2011;Cockell, Rettberg, Rabbow, & Olsson-Francis, 2011) and useful in studies on photosynthesis and nitrogen fixation on early Earth. Most recently, it has been shown to photosynthesise under deeply shaded conditions, utilising chlorophyll f to capture light in the far-red spectrum (Nürnberg et al, 2018).…”

“…The ability to grow endolithically (Büdel et al., ) with high UV resistance (Billi et al., ) would have provided protection to the proposed high UV radiation thought to have existed during the Archaean. Other strategies to overcome UV exposure would have been to grow in shaded areas under rocks (Nürnberg et al., ), in caves (Saw et al., ) or benthically (Heubeck et al., ; Homann et al., ). Salt tolerance would have been necessary for oxygenic phototrophs living in marine and brackish environments (Blank, ).…”