Is a constitutive red-shift an advantage for oxygenic photosynthesis under M dwarf starlight? Insights from <i>Acaryochloris marina</i> sp. str. Moss Beach

Abstract In the next decades, space telescope missions will search for life evidence on exoplanets, focusing on robust biosignatures associated with oxygenic photosynthesis, including atmospheric oxygen accumulation and the Vegetation Red-Edge in surface reflectance spectra. Many habitable rocky exoplanets orbit M dwarf stars, whose spectral energy distribution may condition the rise and evolution of oxygenic photosynthesis. M dwarf stars emit predominantly far-red (700–750 nm) and near-infrared (750–1000 nm) light, and relatively little visible (400–700 nm) radiation, which on Earth predominantly drives photochemistry in most oxygenic phototrophs. Previous experiments proved some oxygenic phototrophs can photosynthesize under simulated M dwarf light but less efficiently than under solar radiation simulated in the range 365-780 nm. Indeed, tested organisms present photosynthetic apparatus evolved to harvest Sun’s visible light, however, M dwarfs’ irradiation might select adaptations optimized for harvesting far-red / near-infrared light. We measured sensitivities of a far-red/near-infrared-utilizing cyanobacterium, Acaryochloris marina sp. str. Moss Beach to simulated M dwarf spectrum and primeval anoxic, CO2-rich atmosphere. This strain constitutively presents a high content of chlorophyll d, with in vivo absorption peak at 710 nm. Its permanently red-shifted photosynthetic apparatus required no acclimation to the stellar spectrum, maintaining strong growth and oxygen production, higher than that registered under simulated solar light. Moreover, abundant chlorophyll d caused a shift in whole-cell reflectance: the red-edge was beyond 700 nm, resulting in a Chl d-near-infrared-edge. Overall, a potentially similar metabolism on exoplanets orbiting M dwarfs could successfully produce both a gaseous biosignature and a characteristic surface biosignature.