Tropical coral reefs are solar-powered oases of marine biodiversity, where scleractinian corals are responsible for building the reef structures that host over 30% of all named marine multicellular species (Fisher et al., 2015). Corals rely heavily on photosynthesis by their dinoflagellate endosymbionts (Symbiodiniaceae) to meet their metabolic requirements (Muscatine, 1990). The distribution of reef-building corals is therefore constrained by the availability of photosynthetically active radiation (PAR, 400–700 nm), which is in turn determined by physical factors such as latitude, seasonality, water depth, and the optical properties of the water body (Kirk, 1994; Kleypas et al., 1999; López-Londoño et al., 2021). Variability in these parameters affects both the quantity and spectral quality of irradiance, exposing corals to a large range of light environments even across small spatial scales (Anthony and Hoegh-Guldberg, 2003; Brakel, 1979; Eyal et al., 2015). On shallow reef flats in clear water regions, corals are routinely exposed to excess irradiance that supersaturates symbiont photosynthesis (Jimenez et al., 2012; Wangpraseurt et al., 2014b), with short light flashes reaching over 3900 µmol photons m^–2 s^–1 due to the lensing effect of waves (Veal et al., 2010). Additionally, shallow-water corals are exposed to a broad irradiance spectrum covering UV to near infrared radiation (Wangpraseurt et al., 2014b). At the other extreme end of the scale, photosynthetic corals on mesophotic reefs at water depths between 50 and 150 m can receive as little as 1% of surface PAR, largely concentrated in the blue-green region of the spectrum and greatly reduced for UV and red wavebands (Eyal et al., 2015; Lesser et al., 2009; Tamir et al., 2019). Light conditions can also vary for individual colonies from the same water depth depending on colony morphology (Kaniewska et al., 2011; Wangpraseurt et al., 2014b) and the reef structure that surrounds them (Falkowski and Dubinsky, 1981; Wangpraseurt et al., 2014b).

Corals have evolved a number of mechanisms for optimising symbiont photosynthesis in the presence of spatial and temporal heterogeneity in light availability. Some of these mechanisms occur at the symbiont cell level, while others involve changes in the coral colony morphology and polyp behaviour (Hoogenboom et al., 2008; Kahng et al., 2019; Kaniewska et al., 2013; Kaniewska and Sampayo, 2022; Kramer et al., 2021; Levy et al., 2003; Todd, 2008). Coral symbionts can modify their light harvesting and energy quenching over timescales ranging from seconds to months. For example, non-photochemical quenching allows rapid dissipation of excess irradiance in the photosynthetic apparatus of symbionts, preventing photodamage in high light environments (Einbinder et al., 2016; Gorbunov et al., 2001; Hoegh-Guldberg and Jones, 1999).

Coral symbionts associated with deeper-water colonies have been frequently found to differ from their shallow-water counterparts in terms of photosystem II photochemical efficiency, maximum electron transport rates, and the organisation of light-harvesting antennae (Einbinder et al., 2016; Hennige et al., 2008; Lohr et al., 2019).

Photosynthetic pigment concentrations and symbiont cell numbers are dynamic within coral colonies, enabling them to acclimate to changes in irradiance; specifically, corals can increase their symbiont numbers as well as the per cell photosynthetic pigment content in response to a reduction in light levels and vice versa (Eyal et al., 2019; Falkowski and Dubinsky, 1981; Martinez et al., 2020; Tamir et al., 2020; Titlyanov et al., 2001). Symbiont community composition within colonies is also known to vary along light and temperature gradients, although the plasticity of this association and the extent to which it can contribute to photoacclimation appears to be species-specific (Chan et al., 2009; Leydet and Hellberg, 2016; Einbinder et al., 2016; Kaniewska and Sampayo, 2022; Lesser et al., 2010; Martinez et al., 2020; Nir et al., 2011; Winters et al., 2009). The interplay between light and temperature is also likely to play a role in shaping these communities on mesophotic reefs (Kahng et al., 2019; Kahng and Kelley, 2007), as the low temperatures sometimes encountered at depth affect the photosynthetic rates of symbiont species differently (Grégoire et al., 2017).

Coral host morphology is an important factor controlling the irradiance available for symbiont photosynthesis (Einbinder et al., 2009; Helmuth et al., 1997; Kahng et al., 2019; Kahng et al., 2012; Kaniewska et al., 2011; Kaniewska and Sampayo, 2022; Nir et al., 2011; Ralph et al., 2002; Wangpraseurt et al., 2014b). Coral colonies from low light environments maximise absorption of downwelling light and assume horizontal plate-like morphologies that promote light collection, while shallow-water colonies assume self-shading morphologies, such as vertical plates or branches (Anthony et al., 2005; Kaniewska et al., 2011). Morphological adaptations make some species depth-specialists, such as the mesophotic coral Leptoseris, which can host photosynthetic symbionts down to depths of well over 100 m (Kahng et al., 2020; Rouzé et al., 2021). Depth-generalist corals on the other hand, such as Montastraea cavernosa in the Caribbean, thrive across light gradients of several orders of magnitude (Lesser et al., 2010). These corals often assume different morphologies in different light environments, allowing a single species to occupy a wider environmental niche. On mesophotic reefs, for instance, the depth-generalist corals Paramontastrea peresi and Porites lobata have growth forms that enhance light exposure, and their skeletons have higher reflectivity compared to their shallow water conspecifics, resulting in higher absorption by the symbionts (Kramer et al., 2020). Such morphological differences are partially due to phenotypic plasticity, as shown by transplantation experiments across depth gradients (Muko et al., 2000; Willis, 1985). However, the relationship between light and colony morphology is not always predictable (Doszpot et al., 2019) as other environmental variables such as hydrodynamics also affect colony morphology (Soto et al., 2018).

Light availability to the coral symbionts depends on the optical properties of the surrounding host tissue and the underlying skeleton (Marcelino et al., 2013; Wangpraseurt et al., 2019; Wangpraseurt et al., 2012). Coral tissue and skeleton scatter incident light with a strength and directionality that are highly variable across species and even between different structures within a single colony (Enríquez et al., 2017; Marcelino et al., 2013; Wangpraseurt et al., 2019; Wangpraseurt et al., 2016a). The interplay between tissue and skeleton scattering/reflection and algal absorption modulate coral photosynthesis (Brodersen et al., 2014; Marcelino et al., 2013; Scheufen et al., 2017; Wangpraseurt et al., 2019). This can lead to outstanding photosynthetic quantum efficiencies that are close to the theoretical maximum, at least for the coral species for which this parameter has been investigated (Brodersen et al., 2014).

Aside from variability in skeletal morphology, tissue-level changes such as contraction and expansion are known to affect light penetration (Wangpraseurt et al., 2014a; Wangpraseurt et al., 2017b). The thickness and composition of the tissue can be affected by a number of variables, including genotype, nutritional status, seasonality, and environmental history (Harland et al., 1992; Jones et al., 2020; Leinbach et al., 2021; Lough and Barnes, 2000; Rocker et al., 2019). Changes in tissue composition (e.g. lipids, collagen, and proteins) will affect the light-scattering properties of the bulk tissue (Jacques, 2013), although detailed investigations on coral optical properties in relation to tissue composition and nutrient status remain to be performed (Lyndby et al., 2019).

The coral host can also modulate incident light by synthesising host pigments. The most widespread coral host pigments belong to the green fluorescent protein (GFP)-like superfamily, a group of homologous pigments which are ubiquitous among the Cnidaria (Alieva et al., 2008; Matz et al., 1999; Shimomura et al., 1962). Pigments in this family share a similar structure based on a tripeptide chromophore capable of absorbing visible or UV radiation (Nienhaus and Wiedenmann, 2009). However, despite having similar structure, cnidarian GFP-like proteins exhibit great variability in their optical properties and regulation mechanisms, indicating that they are functionally diverse (Aihara et al., 2019; Alieva et al., 2008; D’Angelo et al., 2008; Leutenegger et al., 2007; Nienhaus and Wiedenmann, 2009; Salih et al., 2000; Smith et al., 2013).

GFP-like proteins with light-induced expression are found predominantly in corals from high-light environments, and they are transcriptionally regulated by blue-light intensity (D’Angelo et al., 2008; Salih et al., 2000). GFP-like proteins with light-induced expression include fluorescent proteins (FPs) with emission in the cyan, green, and red spectral regions (cyan fluorescent proteins [CFPs], GFPs, and red fluorescent proteins [RFPs]), which absorb light and re-emit it as red-shifted radiation, and non-fluorescent chromoproteins (CPs), which absorb light but have no or little fluorescence emission (Alieva et al., 2008; D’Angelo et al., 2008). These pigments accumulate in high concentration in colony parts with low symbiont densities, often areas of active growth, such as skeletal ridges, the tips of branching corals, the margins of plating corals, and areas affected by epibionts and mechanical damage (D’Angelo et al., 2012a; Salih et al., 2000). The increased photon fluxes inside the host tissue caused by the absence of light absorption by the symbionts, and light reflection and scattering by skeleton and host tissue components (Enríquez et al., 2005; Wangpraseurt et al., 2017a) have been suggested to cause the high-level pigment expression in these colony parts (Bollati et al., 2020; Smith et al., 2013). Additionally, blue light-induced upregulation as part of an optical feedback loop has been shown to drive strong accumulation of these pigments in bleached corals during episodes of mild heat stress or in heat-free bleaching, caused, for instance, by nutrient stress (Bollati et al., 2020; Wiedenmann et al., 2013).

FPs and CPs with light-induced expression are usually localised ectodermally and have been shown to exert a photoprotective function on the underlying symbiont layer (Gittins et al., 2015; Quick et al., 2018; Salih et al., 2000; Smith et al., 2013). Upregulation of these pigments in growing parts of colonies and in bleached tissue has been proposed to promote (re)colonisation of host tissue by symbiont cells via the reduction of internal light stress in areas with low symbiont densities (Bollati et al., 2020; D’Angelo et al., 2012a; Smith et al., 2013).

GFP-like proteins are also widely distributed in corals that are depth generalists or even mesophotic specialists (Eyal et al., 2015; Oswald et al., 2007), where they are constitutively expressed, often at high levels, across a wide range of irradiance regimes (Leutenegger et al., 2007). It has long been proposed that fluorescent pigments in low light habitats could enhance coral photosynthesis by modulating the spectrum and intensity of light that reaches the symbiont cells (Salih et al., 2000; Schlichter et al., 1994). A light-enhancement mechanism has been suggested for a particular group of constitutive GFP-like proteins known as photoconvertible RFPs (pcRFPs), which are common in thick-tissue depth generalist and mesophotic coral species (Ando et al., 2002; Eyal et al., 2015; Oswald et al., 2007; Wiedenmann et al., 2004). pcRFPs emit green fluorescence when first synthesised, but their chromophores are irreversibly converted to a red-emitting species upon absorption of a near-UV photon ~390 nm (Ando et al., 2002; Wiedenmann et al., 2004). As coral GFP-like proteins are typically arranged in tetramers, near-UV-induced post-translational modification leads to the formation of tetramers that contain both green and red subunits; they can therefore absorb light in the blue-green range and re-emit it in the orange-red range via highly efficient Förster resonance energy transfer between adjacent subunits (Bollati et al., 2017; Wiedenmann et al., 2004). The orange-red waveband is scarce on mesophotic reefs, yet it can stimulate chlorophyll fluorescence deeper in the tissue compared to blue-green wavelengths because it is poorly absorbed by photosynthetic pigments, an effect analogous to green light-driven photosynthesis in plant leaves (de Mooij et al., 2016; Smith et al., 2017; Vogelmann and Evans, 2002). Indeed, pcRFP-containing corals have been shown to survive better under a simulated mesophotic light spectrum as compared to non-pigmented conspecifics (Smith et al., 2017).

While GFP-like proteins are likely to have additional functions for the coral holobiont (Aihara et al., 2019; Ben-Zvi et al., 2022; Yamashita et al., 2021), optimisation of the symbiont light environment is arguably one of their primary roles. The effects of GFP-like proteins on the light environment experienced by coral symbionts are not simply dependent on the spectral properties of the isolated protein; rather, they are a product of the environmental and physiological regulation of the protein within its three-dimensional optical context. For example, microsensor measurements and optical modelling have shown that scattering by GFP-like proteins can enhance light penetration at low GFP concentrations, while high concentrations of GFP increase backscattering and reduce light penetration through the coral tissue (Lyndby et al., 2016; Taylor Parkins et al., 2021). Variability in the distribution and arrangement of these proteins – diffuse or granular and ectodermal or endodermal – also affects how they interact with light (Salih et al., 2000; Wangpraseurt et al., 2019), further indicating that spectrally similar GFP-like proteins can be involved in different light modulation mechanisms.

While compelling, the vast majority of evidence provided so far to support the role of GFP-like proteins in modulating the coral photosymbiont light environment during photoacclimation is indirect. This includes light measurements taken outside of the coral tissue (Smith et al., 2017; Smith et al., 2013), optical simulations (Lyndby et al., 2016), and experiments performed on coral-related animals (e.g. corallimorpharians) and isolated symbionts (Smith et al., 2017; Smith et al., 2013). So far, quantitative in vivo and in situ measurements of the symbiont light environment in response to light-driven changes in host pigment composition have been lacking. Here, we used advanced optical sensor technology to directly quantify how light-driven regulation of GFP-like proteins affects the intra-tissue light microenvironment of depth-generalist and shallow-water corals. We focused on the effects of (i) near-UV-driven photoconversion in corals containing pcRFPs, and (ii) blue light-driven upregulation of inducible CPs during bleaching and in active growth zones. Our study provides an essential step towards understanding the role of these pigments in optimising the functioning of the coral-algal symbiosis under extreme light regimes.

Data used in this study is available from https://doi.org/10.5061/dryad.0gb5mkm1z.

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Author details

1. Elena Bollati

   1. Coral Reef Laboratory, School of Ocean and Earth Science, University of Southampton, Southampton, United Kingdom
   2. Marine Biology Section, Department of Biology, University of Copenhagen, Helsingør, Denmark
   3. Department of Biological Sciences, National University of Singapore, Singapore, Singapore

   Contribution

   Formal analysis, Investigation, Visualization, Writing - original draft

   For correspondence

   elena.bollati@bio.ku.dk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3536-4587

2. Niclas H Lyndby

   1. Marine Biology Section, Department of Biology, University of Copenhagen, Helsingør, Denmark
   2. Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0533-9663

3. Cecilia D'Angelo

   Coral Reef Laboratory, School of Ocean and Earth Science, University of Southampton, Southampton, United Kingdom

   Contribution

   Conceptualization, Supervision, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

4. Michael Kühl

   1. Marine Biology Section, Department of Biology, University of Copenhagen, Helsingør, Denmark
   2. Climate Change Cluster, University of Technology Sydney, Sydney, Australia

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1792-4790

5. Jörg Wiedenmann

   Coral Reef Laboratory, School of Ocean and Earth Science, University of Southampton, Southampton, United Kingdom

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2128-2943

6. Daniel Wangpraseurt

   1. Department of NanoEngineering, UC San Diego, San Diego, United States
   2. Marine Biological Research Division, Scripps Institution of Oceanography, UC San Diego, San Diego, United States
   3. Bioinspired Photonics Group, Department of Chemistry, University of Cambridge, Cambridge, United Kingdom

   Contribution

   Conceptualization, Supervision, Investigation, Methodology, Writing – review and editing

   For correspondence

   dwangpraseurt@eng.ucsd.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4834-8981

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