Green fluorescent protein-like pigments optimise the internal light environment in symbiotic reef-building corals

Abstract

Pigments homologous to the Green Fluorescent Protein (GFP) have been proposed to fine-tune the internal light microclimate of corals, facilitating photoacclimation of photosynthetic coral symbionts (Symbiodiniaceae) to life in different reef habitats and environmental conditions. However, direct measurements of the in vivo light conditions inside the coral tissue supporting this conclusion are lacking. Here, we quantified the intra-tissue spectral light environment of corals expressing GFP-like proteins from widely different light regimes. We focus on (1) photoconvertible red fluorescent proteins (pcRFPs), thought to enhance photosynthesis in mesophotic habitats via wavelength conversion, and (2) chromoproteins (CPs), which provide photoprotection to the symbionts in shallow water via light absorption. Optical microsensor measurements indicated that both pigment groups strongly alter the coral tissue light environment. Estimates derived from light spectra measured in pcRFP-containing corals showed that fluorescence emission can contribute to >50% of orange-red light available to the photosynthetic symbionts at mesophotic depths. We further show that upregulation of pink CPs in shallow-water corals during bleaching leads to a reduction of orange light by 10-20% compared to low-CP tissue. Thus, screening by CPs has an important role in mitigating the light-enhancing effect of coral tissue scattering during bleaching. Our results provide the first experimental quantification of the importance of GFP-like proteins in fine-tuning the light microclimate of corals during photoacclimation.

The mesoglea buffers the physico-chemical microenvironment of photosymbionts in the upside-down jellyfishCassiopeasp

“…There has been a special focus on coral skeletons and host pigments (e.g. Falkowski et al, 1984; Kühl et al, 1995; Wangpraseurt et al, 2014b; Lyndby et al, 2019; Kramer et al, 2021; Bollati et al, 2022). Studies have shown that in vivo light exposure of symbionts is modulated on a holobiont level to enhance photosynthesis, including alleviating photodamage and bleaching (Lesser and Farrell, 2004; Enriquez et al, 2005; Marcelino et al, 2013; Wangpraseurt et al, 2017), altering inter- and intracellular pH (e.g.…”

Modulation of the symbionts light environment in hospite in scleractinian corals

“…The upregulation of animal chromoproteins (CPs) in the animal tissue, which is responsible for creating "colorful" bleached corals (Bollati et al, 2020;Bollati et al, 2022), has been proposed as one of the mechanisms for coral bleaching recovery. The most common group of animal CPs found in corals are the Green Fluorescent Proteins (GFP) (Matz et al, 1999;Salih et al, 2000;Alieva et al, 2008;Smith et al, 2013).…”

“…The most common group of animal CPs found in corals are the Green Fluorescent Proteins (GFP) (Matz et al, 1999;Salih et al, 2000;Alieva et al, 2008;Smith et al, 2013). They are primarily found in populations of shallow areas, exposed to high-light environments, and their upregulation can be promoted by blue light (Salih et al, 2000;D'Angelo et al, 2008), nutrient stress (Bollati et al, 2022), and exposure to mild heat stress (Bollati et al, 2020). Animal CPs generally accumulate in parts of the coral colony with low symbiont density composition, such as the areas with the highest growth rate, or parts that are particularly damaged (Smith et al, 2013;Bollati et al, 2020).…”

“…Based on their optical properties, animal CPs can be classified as fluorescent proteins (FPs) and non-fluorescent chromoproteins (CPs) (Alieva et al, 2008). FPs can reemit light at particular wavelengths, a process known as photoconversion (Dove et al, 2001;D'Angelo et al, 2008;Smith et al, 2013;Bollati et al, 2022). Hence, it has been suggested that animal CPs could enhance algal photosynthesis in low light environments by modifying the light spectrum and intensity (Schlichter et al, 1994;Salih et al, 2000;Bollati et al, 2022).…”

“…FPs can reemit light at particular wavelengths, a process known as photoconversion (Dove et al, 2001;D'Angelo et al, 2008;Smith et al, 2013;Bollati et al, 2022). Hence, it has been suggested that animal CPs could enhance algal photosynthesis in low light environments by modifying the light spectrum and intensity (Schlichter et al, 1994;Salih et al, 2000;Bollati et al, 2022). Nevertheless, considering that the number of photons generated through photoconversion is minimal compared to ambient light, its contribution to photosynthesis may be negligible (Ben-Zvi et al, 2021;Bollati et al, 2022).…”