Abstract
Far-red absorbing chlorophylls are constitutively present as chlorophyll (Chl) d in the cyanobacterium Acaryochloris marina, or dynamically expressed by synthesis of Chl f, red-shifted phycobiliproteins and minor amounts of Chl d via far-red light photoacclimation in a range of cyanobacteria, which enables them to use near-infrared-radiation (NIR) for oxygenic photosynthesis. While the biochemistry and molecular physiology of Chl f-containing cyanobacteria has been unraveled in culture studies, their ecological significance remains unexplored and no data on their in situ activity exist. With a novel combination of hyperspectral imaging, confocal laser scanning microscopy, and nanoparticle-based O2 imaging, we demonstrate substantial NIR-driven oxygenic photosynthesis by endolithic, Chl f-containing cyanobacteria within natural beachrock biofilms that are widespread on (sub)tropical coastlines. This indicates an important role of NIR-driven oxygenic photosynthesis in primary production of endolithic and other shaded habitats.
Highlights
Far-red absorbing chlorophylls are constitutively present as chlorophyll (Chl) d in the cyanobacterium Acaryochloris marina, or dynamically expressed by synthesis of Chl f, red-shifted phycobiliproteins and minor amounts of Chl d via far-red light photoacclimation in a range of cyanobacteria, which enables them to use near-infrared-radiation (NIR) for oxygenic photosynthesis
Hyperspectral reflectance imaging on vertical cross-sections of beachrock submerged in seawater (23 ̊C and salinity = 35) revealed the presence of a dense ~1 mm thick surface biofilm with high amounts of Chl a, while a more patchy zone containing Chl f, and less Chl a was found below the Figure 1 continued on page
Based on O2 concentration images recorded at 5 min intervals after experimental light-dark shifts, we calculated images of apparent dark respiration and NIR-driven net and gross photosynthesis that could be mapped onto the beachrock structure (Figure 2A–D) showing that hotspots of activity aligned with the presence of Chl f
Summary
The persisting textbook notion that oxygenic photosynthesis is mainly driven by visible wavelengths of light (400–700 nm) and chlorophyll (Chl) a as the major photopigment is challenged; recent findings indicate that cyanobacteria with red-shifted chlorophylls and phycobiliproteins capable of harvesting near-infrared-radiation (NIR) at wavelengths > 700–760 nm and exhibiting a pronounced plasticity in their photoacclimatory responses (Gan et al, 2014; Gan and Bryant, 2015) are widespread in natural habitats (Gan et al, 2015; Zhang et al, 2019; Behrendt et al, 2019). With a novel combination of hyperspectral imaging, confocal laser scanning microscopy, and nanoparticle-based O2 imaging, we demonstrate substantial NIR-driven oxygenic photosynthesis by endolithic, Chl f-containing cyanobacteria within natural beachrock biofilms that are widespread on (sub)tropical coastlines.
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