How cyanobacteria use ‘leftover’ light in shaded environments

Photosynthetic light harvesting lies at the crossroads of two equally important needs: covering the largest portion of the solar spectrum and achieving the highest yields of energy conversion. Some cyanobacteria living in shaded environments can teach us how to trick this balance to our advantage.

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Oxygenic photosynthesis sustains life on Earth by converting visible light into chemical energy. Cyanobacteria are the main responsible for the oxygenation of our atmosphere. They populate a huge variety of environments, ranging from hot springs to marine and fresh waters, from soil crusts to polar icecaps and are therefore invaluable primary producers in many ecosystems.

Cyanobacteria, as well as algae and plants, use their chlorophyll-reach photosystems to carry out the first steps of the light to chemical energy transduction. Photosystems are membrane-embedded complexes of proteins, pigments and electron carriers that harvest light and use its energy to drive charge separation. The latter event, similar to what happens at the poles of a battery, triggers all following photosynthetic electrochemical reactions. Due to their light-dependency, the rate of these processes increases concomitantly with the number of absorbed photons. Not all solar photons, however, are equally effective at powering these reactions and photosynthetic yields substantially drop in the infra-red spectral region. This is the reason why oxygenic photosynthesis relies near universally on chlorophyll a, the well-known green pigment absorbing light in the 400-700 nm range (which roughly corresponds to the visible light spectrum). As a result, the wavelengths above 700 nm, representing over 50% of the total solar irradiance, remain largely unutilized. The spectral restrictions imposed by the use of chlorophyll a can be particularly limiting under the shade of a dense plant canopy, where most visible light is absorbed by the upper leaves. Therefore, pushing the light-harvesting capacity beyond these natural limits represents an appealing approach for increasing biomass yields.

An intuitive strategy for extending the photosynthetic active spectrum is to select pigments absorbing at longer wavelengths (or, equivalently, lower energies) than chlorophyll a. In this respect, a lesson from nature comes from some recently discovered cyanobacterial species that populate deep shaded environments. These strains can adapt to use the longer wavelength “leftover” light by remodeling their photosynthetic apparatus and synthesizing a different pigment, chlorophyll f. Though chlorophyll f makes these cyanobacteria capable of capturing photons with wavelengths between 700-800 nm, very little was known so far about its impact on the photosynthetic performances. This information is essential if we wish to introduce this pigment into other organisms, such as plants and algae, to expand their light-harvesting capacity.

In this work, by studying the ultra-fast processes that follow light absorption by the photosystems (typically on a sub-nanosecond timescale), we found that the presence of chlorophyll f slows down charge separation. Although this can sometimes reduce the efficiency of the photosystems, the use of chlorophyll f remains beneficial in shaded environments that are highly enriched in low-energy photons, where chlorophyll a would hardly absorb any light. This finding proves that the use of chlorophyll f is a viable strategy for extending the absorption spectrum of engineered crops. Our analyses also shed light on the structural and energetic reasons behind the reduced performances of chlorophyll f-containing photosystems. This way, we provide a starting point for the rational design of new photosynthetic units that is required to achieve the desired high biomass yields.

To read the full story, please check our publication on Nature Plants at the link: https://www.nature.com/articles/s41477-020-0718-z

Left panel: 3D structure of monomeric Photosystem I from the cyanobacterium Fischerella thermalis acclimated to near IR light [1]. The protein is shown in transparent grey, chlorophyll a pigments in solid green, and chlorophyll f pigments in solid red. Note that near-IR-absorbing chlorophyll f pigments represent only a sub-population of all chlorophylls. Right panel: flux of solar photons at the Earth’s surface (photons per unit surface and time, in arbitrary scale) across the electromagnetic spectrum (top) and its magnification in the visible and near IR region (bottom). The bottom right graph shows the wavelength-dependent light spectrum in full sun (daylight, yellow) and under a dense leaf canopy (brown) [2]. The latter is enriched in near IR wavelengths (above 700 nm). The spectral ranges of chlorophyll a and chlorophyll f are also indicated.

[1] Gisriel, C. et al. The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis. Sci. Adv. 6, eaay6415 (2020).

[2] Gan, F. & Bryant, D. A. Adaptive and acclimative responses of cyanobacteria to far-red light. Environ. Microbiol. 17, 3450–3465 (2015).

Vincenzo Mascoli

PhD student, Vrije Universiteit Amsterdam

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