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Summary Symbiosis between eukaryotic microalgae and heterotrophic hosts is a widespread, phylogenetically convergent, and ecologically important phenomenon in aquatic ecosystems. Partners include taxonomically diverse microalgae interacting with multicellular or unicellular hosts in marine or freshwater environments. While progress has been made recently, there are still major knowledge gaps on the microenvironmental conditions of microalgaein hospite(e.g. nutrient and CO₂availability), the algal carbon metabolism (production and storage), and the cellular mechanisms of carbohydrate export to the host. This review aims to provide current knowledge on the physiology and metabolism of symbiotic microalgae, to highlight whether there are commonalities across different photosymbioses, and to identify new approaches and technologies for disentangling photosymbiotic interactions at relevant temporal and spatial scales. 

The upside-down jellyfish, Cassiopea spp., host their algal symbionts inside a subset of amoebocytes, phagocytic cells that also play innate immune functions akin to macrophages from vertebrate animals. Amoebocyte precursors phagocytose algae from the jellyfish gut and store them inside intracellular compartments called symbiosomes. Subsequently, the precursors migrate to the mesoglea, differentiate into symbiotic amoebocytes, and roam throughout the jellyfish body where the algae remain photosynthetically active and supply the jellyfish host with a significant portion of their organic carbon needs. Here, we show that the amoebocyte symbiosome membrane contains V-H+-ATPase (VHA), the proton pump that acidifies phagosomes and lysosomes in all eukaryotes. Many symbiotic amoebocytes also abundantly express a carbonic anhydrase (CA), an enzyme that reversibly hydrates CO2 into H+ and HCO3−. Moreover, we found that the symbiosome lumen is pronouncedly acidic and that pharmacological inhibition of VHA or CA activities significantly decreases photosynthetic oxygen production in live jellyfish. These results point to a carbon concentrating mechanism (CCM) that co-opts VHA and CA from the phago-lysosomal machinery that ubiquitously mediates food digestion and innate immune responses. Analogous VHA-dependent CCMs have been previously described in reef-building corals, anemones, and giant clams; however, these other two cnidarians host their dinoflagellate algae inside gastrodermal cells -not in amoebocytes- and the clam hosts theirs within the gut lumen. Thus, our study identifies an example of convergent evolution at the cellular level that might broadly apply to invertebrate-microbe photosymbioses while also providing evolutionary links with intra- and extracellular food digestion and the immune system. 

Rapid progress in algal biotechnology has triggered a growing interest in hydrogel-encapsulated microalgal cultivation, especially for the engineering of functional photosynthetic materials and biomass production. An overlooked characteristic of gel-encapsulated cultures is the emergence of cell aggregates, which are the result of the mechanical confinement of the cells. Such aggregates have a dramatic effect on the light management of gel-encapsulated photobioreactors and hence strongly affect the photosynthetic outcome. To evaluate such an effect, we experimentally studied the optical response of hydrogels containing algal aggregates and developed optical simulations to study the resultant light intensity profiles. The simulations are validated experimentally via transmittance measurements using an integrating sphere and aggregate volume analysis with confocal microscopy. Specifically, the heterogeneous distribution of cell aggregates in a hydrogel matrix can increase light penetration while alleviating photoinhibition more effectively than in a flat biofilm. Finally, we demonstrate that light harvesting efficiency can be further enhanced with the introduction of scattering particles within the hydrogel matrix, leading to a fourfold increase in biomass growth. Our study, therefore, highlights a strategy for the design of spatially efficient photosynthetic living materials that have important implications for the engineering of future algal cultivation systems.