Thermodynamic Limits Around M-dwarf Stars: Discussion

Table of Links

• Abstract and Introduction
• 2 Methodology
• 2.1 Local spectral irradiance as a function of stellar temperature
• 2.2 Thermodynamic model of an oxygenic light-harvesting system
• 2.3 Lattice model of an oxygenic light-harvesting system
• 3 Results
• 3.1 Orbital distances and incident spectral fluxes
• 3.2 Thermodynamic antenna model: Increasing antenna size in limited PAR
• 3.3 Lattice antenna model: Increasing the size of a “flat” antenna in limited PAR
• 3.4 Lattice antenna model: Improving antenna efficiency with an energetic ’funnel’
• 4 Discussion
• Acknowledgements, Author Contribution Statement, Authors disclosure statement and References

4 Discussion

The results of our generalized antenna models suggest that the oxygenic photosynthesis is likely feasible on exo-planets orbiting low mass M-dwarf stars, though there are some restrictions. A light-harvesting system similar to PSII of vascular plants (but with a larger antenna) would be severely entropy-limited even before we factor in local limitations like water scarcity, atmospheric attenuation of light, etc. However, this reflects the fact that plants are evolved to deal with highly variable irradiance [Vialet-Chabrand et al., 2017, Li et al., 2021] rather than constant low light. One of the major risks to plants is actually excessive illumination which can cause oxidative damage to PSII, a metabolically costly phenomenon known as photoinhibition, and one that should be familiar to anyone who has suddenly moved a houseplant into full sun. To mitigate photoinhibition [Aro et al., 1993], plants possess regulatory mechanisms that suppress photon absorption and down-regulate the antenna [Ruban, 2016, Ruban and Wilson, 2021]. Therefore it is unsurprising that such a system does not perform well in severely PAR-depleted light. However, by introducing an energetic gradient to the antenna (the energy funnel) we were able to significantly improve antenna efficiency and electron output. Of the branched and hexagonal antenna topologies the former performs better, able to match the performance of the latter but with fewer LHC subunits and a shallower energetic gradient. Fewer LHC subunits is perhaps the most important factor as it is directly related to the metabolic “cost” of the antenna.

Of course, there are countless other modifications that could be made to the antenna. For example, one could increase pigment density which would increase the overall cross-section of each LHC and enhance inter-pigment energy transfer. The pigment concentration in LHCII is already very high, approximately 1 mol dm−3 , and the protein scaffold enforces highly specific inter-pigment distances and relative orientations to avoid dissipative processes such as concentration quenching [Liu et al., 2004]. However, one could imagine an adaptation similar to the chlorosome antenna of green sulphur bacteria [Oostergetel et al., 2010]. This structure is a solid aggregate of ∼ 300, 000 BChls encapsulated in a membrane sheath, effectively the densest pigment packing possible, and it facilitates (anoxygenic) photosynthesis in extremely low illumination. It should be noted however that such as structure is is a significant metabolic investment and one that is not seen in any large multi-cellular organism. Alternatively, one could replace Chl a and b with pigments with larger intrinsic cross-sections and/or absorption widths, which would increase the rate of photon absorption, γi . Since intermolecular energy transfer depends on the oscillator strengths and spectral overlap of the pigments involved, this may also enhance the intrinsic transfer rates, (Ki,j ) −1 . Still, the branched, funnel antenna strategy is a plausible one because it explicitly addresses the fundamental thermodynamic limits inherent in light-harvesting. More importantly, such an antenna actually exists on in Earth in the form of the phycobilisome of oxygenic cyanobacteria [Saer and Blankenship, 2017].

Like our model, the phycobilisome is modular and can adapt to changes in irradiance. Kolodny et al. [2022] recently showed that cyanobacteria in deep water, where light is very blue-shifted, will lenghten their phycobilisome rods by adding more terminal PE subunits and will increase overall antenna efficiency, ϕF , by tuning pigment content (and possibly density). The most important result, however, is the recent work of Battistuzzi et al. [2023] who showed that cyanobacteria could comfortably adapt to the the light typical of M-dwarf stars. Moreover, they used a sophisticated starlight simulator setup which models atmospheric attenuation of light, meaning their cyanobacteria were likely subject to ever scanter illumination than we consider here. Interestingly, they also considered pure “far red” (700−800 nm) illumination and found that this retarded growth rate relative to the M-dwarf light, implying that, as in our model, the organism was adapting its antenna to intercept more photons in the depleted PAR region.It should be noted that they also considered on the red-adapted strains described in the introduction that fared equally well in M-dwarf and far red light.

Strictly, both our modelling and the experimental work of Kolodny et al. [2022]. concerns the acclimation of an existing antenna to an unusual lightenvironment rather than the ground-up evolution of an antenna structure specifically optimized to it. Nevertheless, Kolodny’s work demonstrates that oxygenic photosynthesis is, in principle, possible around very low mass stars and our findings indicate that the key consideration is overcoming a fundamental entropic barrier to light-harvesting.