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© 2018 Rädecker, Raina, Pernice, Perna, Guagliardo, Kilburn, Aranda and Voolstra. The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis, yet has proven difficult given the endosymbiotic nature of this relationship. In this study, we investigated the respective contribution of host and symbiont to carbon and nitrogen assimilation in the coral model anemone Aiptaisa. For this, we combined traditional measurements with nanoscale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling to investigate patterns of nutrient uptake and translocation both at the organismal scale and at the cellular scale. Our results show that the rate of carbon and nitrogen assimilation in Aiptasia depends on the identity of the host and the symbiont. NanoSIMS analysis confirmed that both host and symbiont incorporated carbon and nitrogen into their cells, implying a rapid uptake and cycling of nutrients in this symbiotic relationship. Gross carbon fixation was highest in Aiptasia associated with their native Symbiodinium communities. However, differences in fixation rates were only reflected in the δ13C enrichment of the cnidarian host, whereas the algal symbiont showed stable enrichment levels regardless of host identity. Thereby, our results point toward a "selfish" character of the cnidarian-Symbiodinium association in which both partners directly compete for available resources. Consequently, this symbiosis may be inherently instable and highly susceptible to environmental change. While questions remain regarding the underlying cellular controls of nutrient exchange and the nature of metabolites involved, the approach outlined in this study constitutes a powerful toolset to address these questions.

Metarhizium robertsii is a common soil fungus that occupies a specialized ecological niche as an endophyte and an insect pathogen. Previously, we showed that the endophytic capability and insect pathogenicity of Metarhizium are coupled to provide an active method of insect-derived nitrogen transfer to a host plant via fungal mycelia. We speculated that in exchange for this insect-derived nitrogen, the plant would provide photosynthate to the fungus. By using 13CO2, we show the incorporation of 13C into photosynthate and the subsequent translocation of 13C into fungal-specific carbohydrates (trehalose and chitin) in the root/endophyte complex. We determined the amount of 13C present in root-associated fungal biomass over a 21-day period by extracting fungal carbohydrates and analysing their composition using nuclear magnetic resonance (NMR) spectroscopy. These findings are evidence that the host plant is providing photosynthate to the fungus, likely in exchange for insect-derived nitrogen in a tripartite, and symbiotic, interaction., The endophytic fungus Metarhizium robertsii is also an insect pathogen and can facilitate transfer of insect-derived nitrogen to host plants. Here, the authors show that carbon is transferred from plant to fungus suggesting a tripartite interaction where nitrogen is exchanged for photosynthate.

The coral symbiosis is the linchpin of the reef ecosystem, yet the mechanisms that promote and maintain cooperation between hosts and symbionts have not been fully resolved. We used a phylogenetically controlled design to investigate the role of vertical symbiont transmission, an evolutionary mechanism in which symbionts are inherited directly from parents, predicted to enhance cooperation and holobiont fitness. Six species of coral, three vertical transmitters and their closest horizontally transmitting relatives, which exhibit environmental acquisition of symbionts, were fragmented and subjected to a two-week thermal stress experiment. Symbiont cell density, photosynthetic function and translocation of photosynthetically fixed carbon between symbionts and hosts were quantified to assess changes in physiological performance and cooperation. All species exhibited similar decreases in symbiont cell density and net photosynthesis in response to elevated temperature, consistent with the onset of bleaching. Yet baseline cooperation, i.e. translocation of photosynthate, in ambient conditions and the reduction in cooperation in response to elevated temperature differed among species. Although Porites lobata and Galaxea acrhelia did exhibit the highest levels of baseline cooperation, we did not observe universally higher levels of cooperation in vertically transmitting species. Post hoc sequencing of the Symbiodinium ITS-2 locus was used to investigate the potential role of differences in symbiont community composition. Interestingly, reductions in cooperation at the onset of bleaching tended to be associated with increased symbiont community diversity among coral species. The theoretical benefits of evolving vertical transmission are based on the underlying assumption that the host-symbiont relationship becomes genetically uniform, thereby reducing competition among symbionts. Taken together, our results suggest that it may not be vertical transmission per se that influences host-symbiont cooperation, but genetic uniformity of the symbiont community, although additional work is needed to test this hypothesis.

In Crocus vernus, a spring bulbous species, prolonged growth at low temperatures results in the development of larger perennial organs and delayed foliar senescence. Because corm growth is known to stop before the first visual sign of leaf senescence, it is clear that factors other than leaf duration alone determine final corm size. The aim of this study was to determine whether reduced growth at higher temperatures was due to decreased carbon import to the corm or to changes in the partitioning of this carbon once it had reached the corm. Plants were grown under two temperature regimes and the amount of carbon fixed, transported, and converted into a storable form in the corm, as well as the partitioning into soluble carbohydrates, starch, and the cell wall, were monitored during the growth cycle. The reduced growth at higher temperature could not be explained by a restriction in carbon supply or by a reduced ability to convert the carbon into starch. However, under the higher temperature regime, the plant allocated more carbon to cell wall material, and the amount of glucose within the corm declined earlier in the season. Hexose to sucrose ratios might control the duration of corm growth in C. vernus by influencing the timing of the cell division, elongation, and maturation phases. It is suggested that it is this shift in carbon partitioning, not limited carbon supply or leaf duration, which is responsible for the smaller final biomass of the corm at higher temperatures.

Background It was recently discovered that symbiotic algae in the eggs of the salamander Ambystoma maculatum translocate fixed carbon from photosynthesis to developing embryos. Fixed carbon translocation was shown in embryos at one time point during development, however, it was unknown if fixed carbon translocation occurs throughout all developmental stages. Findings In this study, fixed carbon translocation was measured in salamander eggs at six time points over the latter half of development. Fixed carbon translocation did not occur until the middle tailbud portion of development (stages 26–30), and translocation was measured in 20% or less of eggs sampled. Peak carbon translocation occurred during the late tailbud phase of development (stages 31–35), where as much as 87% of eggs sampled showed translocation, and average percent translocation was 6.5%. During the final stages of development, fixed carbon translocation declined, and translocation was not detected in embryos five days prior to hatching. Conclusions The onset of fixed carbon translocation from Oophila to A. maculatum embryos during the second half of embryonic development is likely due to the corresponding settlement and concentration of Oophila in the inner egg envelope. In addition, carbon translocation ceases in late stage embryos as the inner egg envelope thins and ruptures in preparation for hatching.

Symbiosis has been an important factor in evolution, and continues to drive speciation and allows organisms to fill new ecological niches. Symbiotic relationships in which both partners benefit from the association, or mutualisms, are ubiquitous in both terrestrial and aquatic ecosystems. Many of the symbionts in these associations are photosynthetic algae or cyanobacteria that fix carbon through photosynthesis and translocate a portion of this energy to their hosts. Host organisms utilize this fixed carbon for a variety of physiological processes, including growth and development, thus, photosynthetically-fixed carbon is vital for many hosts. The following chapters will describe carbon fixation and translocation in two algal symbioses: the freshwater association between the alga Oophila and the eggs of Ambystoma maculatum salmanders, and the relationship between the dinoflagellate Symbiodinium and marine zoanthids. These chapters will discuss carbon flux in symbiosis, and reveal some of the ways in which environmental factors alter photosynthesis in algal mutualisms.