Substantial near-infrared radiation-driven photosynthesis of chlorophyllf-containing cyanobacteria in a natural habitat

Abstract

Far-red absorbing chlorophylls are constitutively present as Chl d in the 14 cyanobacterium Acaryochloris marina, or dynamically expressed by synthesis of Chl f and red-15 shifted phycobilins via far-red light photoacclimation in a range of cyanobacteria, which enables 16 them to use near-infrared-radiation (NIR) for oxygenic photosynthesis. While the biochemistry 17 and molecular physiology of Chl f-containing cyanobacteria has been unraveled in culture 18 studies, their ecological significance remains unexplored and no data on their in situ activity 19 exist. With a novel combination of hyperspectral imaging, confocal laser scanning microscopy, 20 and nanoparticle-based O2 imaging, we demonstrate substantial NIR-driven oxygenic 21 photosynthesis by endolithic, Chl f-containing cyanobacteria within natural beachrock biofilms 22 that are widespread on (sub)tropical coastlines. This indicates an important role of NIR-driven 23 oxygenic photosynthesis in primary production of endolithic and other shaded habitats. 24 25 Impact statement: Cyanobacteria with chlorophyll f show substantial near-infrared radiation-26 driven photosynthesis in intertidal habitats. 27 Behrendt L, Brejnrod A, Schliep M, Sørensen SJ, Larkum AWD, Kühl M. 2015. Chlorophyll f-388 driven photosynthesis in a cavernous cyanobacterium. ISME Journal 9:2108-2111. 389 Behrendt L, Trampe EL, Nord NB, Nguyen J, Lonco D, Nyarko A, Dhinojwala A, Hershey OH, 390 Kühl M, Barton H. 2019. Life in the dark: Far-red absorbing cyanobacteria extend photic 391 zones deep into terrestrial caves. Environmental Microbiology

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

“…Intertidal beachrock habitats are widespread sedimentary features of (sub)tropical coastlines (Vausdaukas et al, 2007) that can harbor endolithic cyanobacteria with Chl f growing under a dense surface biofilm of other cyanobacteria that strongly absorb visible light (Trampe and Kühl 2016). We recently showed a pronounced NIR-driven O 2 production in the Chl f-containing layer of beachrock (Kühl et al 2020), indicating a potential for cyanobacteria with FaRLiP to contribute substantially to primary production. However, these first estimates were hampered by a lack of data on beachrock primary production, and the NIR-driven rates of photosynthesis were estimated from imaging O 2 dynamics in small hot-spots of activity, while illuminating beachrock cross sections homogeneously with a single low irradiance, which may not be representative of the in-situ light levels and differs from the natural, vertical light gradients in beachrock.…”

“…Beachrock samples and pigmentation. Previous studies across the beachrock platform on Heron Island revealed three characteristic biofilm communities predominated by cyanobacteria, as characterized by their surface coloration (black, brown and pink) and microbial community composition (Diez et al 2007;Trampe and Kühl 2016;Kühl et al 2020). The biofilms are characterized by a <1-2 mm thin, optically dense surface layer on top of a more loosely defined, greenish endolithic layer 1-4 mm below the surface of the beachrock (Fig.…”

“…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 Chl f-containing cyanobacteria capable of using NIR for oxygenic photosynthesis (Kühl et al, 2020). Here we use a combination of gas exchange measurements and luminescence lifetimebased O 2 imaging 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.…”

Imaging O2 dynamics and microenvironments in the seagrass leaf phyllosphere with magnetic optical sensor nanoparticles

“…Unfavourable water‐column conditions such as heatwaves and ocean deoxygenation (predicted in future climate scenarios) may exacerbate the occurrence and detrimental effects of these anoxic microniches in the seagrass leaf microenvironment, especially at night, leading to increased die‐off events in exposed areas (Borum et al ., 2005, 2006; Pedersen et al ., 2016). In the subsurface layers of the epiphytic biofilm, hot spots for microbial activity may include shaded microhabitats with high photosynthetic productivity driven by cyanobacteria with chlorophyll d and f using near‐infrared light (>700 nm) for oxygenic photosynthesis (Kühl et al ., 2020). Such ecological niches in the micro‐understory of the epiphytic biofilm could be targeted for pigment analysis and amplicon sequencing (Figure 4; Kühl et al ., 2020), elucidating the potential importance for such shaded microhabitats below the epiphytic microalgal canopies.…”

“…In the subsurface layers of the epiphytic biofilm, hot spots for microbial activity may include shaded microhabitats with high photosynthetic productivity driven by cyanobacteria with chlorophyll d and f using near‐infrared light (>700 nm) for oxygenic photosynthesis (Kühl et al ., 2020). Such ecological niches in the micro‐understory of the epiphytic biofilm could be targeted for pigment analysis and amplicon sequencing (Figure 4; Kühl et al ., 2020), elucidating the potential importance for such shaded microhabitats below the epiphytic microalgal canopies.…”