Near infrared radiation-driven oxygenic photosynthesis contributes substantially to primary production in biofilms harboring chlorophyllf-containing cyanobacteria

Cyanobacteria with far-red light photoacclimation (FaRLiP) can modify their photopigmentation by synthesizing red-shifted phycobiliproteins and chlorophylls, i.e., chlorophyll (Chl)dandf. This enables use of near-infrared radiation (NIR) for oxygenic photosynthesis in habitats depleted of visible light (VIS). Cyanobacteria with FaRLiP are widespread but their quantitative importance for primary production in natural habitats remains unknown. Previously we showed that intertidal beachrock formations can harbor endolithic populations of Chlf-containing cyanobacteria capable of using NIR for oxygenic photosynthesis (Kühl et al., 2020). Here we use a combination of gas exchange measurements and luminescence lifetime-based O₂imaging to quantify how endolithic cyanobacteria with far-red chlorophylls contribute to the primary production of an intertidal beachrock habitat when exposed to a natural gradient of visible and near-infrared radiation. While VIS-driven photosynthesis predominantly took place in the dense cyanobacterial surface biofilm of beachrock, NIR-driven photosynthesis was mainly confined to a subsurface layer in the beachrock containing endolithic cyanobacteria with Chlfandd. Yet such subsurface, NIR-driven photosynthesis provided a substantial O₂production reaching >20% of the gross photosynthesis rates under comparable photon irradiance of visible light. This points to a hitherto overlooked role of far-red light acclimated cyanobacteria for primary production in natural habitats characterized by steep attenuation of visible light and relative enrichment in near-infrared radiation.