Niclas Heidelberg Lyndby | EPFL Graph Search

About this result

This page is automatically generated and may contain information that is not correct, complete, up-to-date, or relevant to your search query. The same applies to every other page on this website. Please make sure to verify the information with EPFL's official sources.

Photobiology and metabolic interactions in the symbiotic jellyfish Cassiopea

Niclas Heidelberg Lyndby

The symbiont-bearing jellyfish Cassiopea live a benthic lifestyle, positioning themselves upside-down on sediments in shallow waters to allow their endosymbiotic algae to photosynthesize in the sunlight. Over the last decades Cassiopea has become increasingly popular as a model system for photosymbiosis because, like reef-building corals, these animals rely on autotrophic assimilation of carbon from its algal symbionts. However, relatively little is still known about the photobiology of Cassiopea. Previous studies have focused on investigations of O2 production or CO2 consumption at the scale of entire individuals. Metabolic interactions between animal host and symbiont algae have been studied with bulk isotopic bulk analyses of host tissue vs. the symbiont population. Yet, this symbiosis is the result of single-cell interactions that are modulated by surrounding tissue microenvironments. Accounting for this cellular and spatial heterogeneity of interactions is thus crucial for advancing our understanding of the photobiology of Cassiopea.Unlike reef-building corals, Cassiopea maintain their symbionts in specialized host cells, the motile amoebocytes, residing in the mesoglea of the animal. In the first chapter of this thesis, I thus explored the role of these cells in the nutrient uptake and exchange between host and symbionts. Stable isotope labelling experiments were combined with correlated scanning electron microscopy and NanoSIMS imaging, to achieve a better understanding of the fate of assimilated carbon and the photosynthate translocation in hospite. Amoebocytes hosting clusters of symbionts were found primarily adjacent to the subumbrella epidermis, and incubation experiments with 13C-bicabonate demonstrated that photosynthates produced by the symbiotic algae are transferred via the amoebocytes to host epidermis. Thus, the amoebocytes facilitate nutrient transfer between host and symbionts, and enable host assimilation of autotrophic carbon. Furthermore, incubations with 15NH4+ and 15NO3- demonstrated that Cassiopea prefer NH4+ as their nitrogen source; assimilation of NO3- was not detected in any of the holobiont compartments investigated here by NanoSIMS imaging. Both the symbiotic algae and the host animal contribute to the assimilation of NH4+. In conclusion, the amoebocytes appear to be a key adaptation for the Cassiopea symbiosis, as they facilitate nutrient transfer in hospite and keeps symbionts near the most light-exposed parts of the bell to optimize photosynthesis. In the second chapter, I investigated the photobiology and physico-chemical microenvironment of Cassiopea using microsensors. Photon scalar irradiance across the medusa was found to be highly heterogenous and light availability was found to be highest at the apical parts (i.e., the oral arms and manubrium) of the animal. Surface reflectance revealed that white granules (spheres of ca. 200 µm in diameter) found in the bell tissue along rhopalia canals strongly scatter light, and scalar irradiance measurements showed that light availability was locally enhanced in tissue containing white granules in high density. Depth profiles of O2 concentrations in the bell mesoglea of large individuals (> 6 cm) revealed increasing concentration of O2 down towards the middle of the mesoglea (i.e., halfway between sub- and exumbrella epidermis), in light reaching levels 2-fold higher than the ambient water. During dark periods, the O2 concentration slowly decreased deep

EPFL2023

The mesoglea buffers the physico-chemical microenvironment of photosymbionts in the upside-down jellyfish Cassiopea sp.

Niclas Heidelberg Lyndby, Anders Meibom

IntroductionThe jellyfish Cassiopea has a conspicuous lifestyle, positioning itself upside-down on sediments in shallow waters thereby exposing its photosynthetic endosymbionts (Symbiodiniaceae) to light. Several studies have shown how the photosymbionts benefit the jellyfish host in terms of nutrition and O-2 availability, but little is known about the internal physico-chemical microenvironment of Cassiopea during light-dark periods. MethodsHere, we used fiber-optic sensors to investigate how light is modulated at the water-tissue interface of Cassiopea sp. and how light is scattered inside host tissue. We additionally used electrochemical and fiber-optic microsensors to investigate the dynamics of O-2 and pH in response to changes in the light availability in intact living specimens of Cassiopea sp. Results and discussionMapping of photon scalar irradiance revealed a distinct spatial heterogeneity over different anatomical structures of the host, where oral arms and the manubrium had overall higher light availability, while shaded parts underneath the oral arms and the bell had less light available. White host pigmentation, especially in the bell tissue, showed higher light availability relative to similar bell tissue without white pigmentation. Microprofiles of scalar irradiance into white pigmented bell tissue showed intense light scattering and enhanced light penetration, while light was rapidly attenuated over the upper 0.5 mm in tissue with symbionts only. Depth profiles of O-2 concentration into bell tissue of live jellyfish showed increasing concentration with depth into the mesoglea, with no apparent saturation point during light periods. O-2 was slowly depleted in the mesoglea in darkness, and O-2 concentration remained higher than ambient water in large (> 6 cm diameter) individuals, even after 50 min in darkness. Light-dark shifts in large medusae showed that the mesoglea slowly turns from a net sink during photoperiods into a net source of O-2 during darkness. In contrast, small medusae showed a more dramatic change in O-2 concentration, with rapid O-2 buildup/consumption in response to light-dark shifts; in a manner similar to corals. These effects on O-2 production/consumption were also reflected in moderate pH fluctuations within the mesoglea. The mesoglea thus buffers O-2 and pH dynamics during dark-periods.

FRONTIERS MEDIA SA2023

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

Niclas Heidelberg Lyndby

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 intra-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 and skeletal reflection 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.

2022