The Influence of Symbiont Diversity on the Functional Biology of a Model Sea Anemone

<p>Cnidarian–dinoflagellate symbioses, particularly those between anthozoans and dinoflagellates of the genus Symbiodinium (commonly referred to as zooxanthellae) are widespread in the marine environment. They are responsible for the formation of coral reefs and are thus of great ecological importance. In recent years there has been an increase in the frequency and severity of episodes of coral bleaching resulting in degradation and mortality of coral reefs on a global scale. In order to gain a deeper understanding of how corals can adapt to changing environmental conditions, the effect that symbiont type has on the persistence and physiology of an association needs to be ascertained. The aim of this research was to determine how different symbiont types affect the nutritional biology and intracellular physiology of the symbiosis when in association with the sea anemone Aiptasia pulchella. The specific objectives of the study were to; (1) determine whether different symbiont types are equally as adept at supporting the energetic demands of the same host; (2) determine if internal pH (pHi) is a reflection of symbiont type and whether the optimal pH for photosynthesis coincides with the host cell pHi; and (3) test the influence of Symbiodinium type on host tissue glycerol and glucose pools. In order to answer these questions, aposymbiotic (i.e. symbiont-free) sea anemones were infected with different Symbiodinium types and the relationship between symbiont type, photosynthetic performance and autotrophic potential was tested. A range of ‘normal’ and novel cnidarian–dinoflagellate symbioses was also used to measure host cell pHi and to determine the optimal pHi of isolated intact symbiosomes (i.e. the vacuoles that house the symbionts), as well as to compare the amounts of free glycerol and glucose (metabolites) present in the host tissues. Different host-symbiont combinations were found to have different photosynthetic and respiratory attributes. Earlier onset of full autotrophy (i.e. when all metabolic carbon demands of the symbiosis were met by photosynthesis) and higher CZAR values (i.e. the contribution of zooxanthellae to animal respiration) were demonstrated by symbioses hosting Symbiodinium B1 both from the original (homologous) and different (heterologous) host. The study showed that Symbiodinium types differ in their pH optima and that the optimal pHi for photosynthesis does not always match the actual measured pHi. Symbiont type was also shown to have an effect on host tissue glycerol and glucose pools, with the associations harbouring the homologous Symbiodinium B1 attaining the highest concentrations of both metabolites. Findings from this study suggest that corals may be able to maintain an association with a range of Symbiodinium types, and hence potentially switch as a consequence of bleaching. The new symbiont type may not be as nutritionally advantageous as the original type however, which could have implications for the growth and survivorship of the coral, unless it is able to supplement its carbon demands heterotrophically. The rapid proliferation of some of the heterologous Symbiodinium types (e.g. Symbiodinium E2) inside the host indicates that, after bleaching, there is potential for fast symbiont establishment. The reduced carbon contribution of these heterologous symbionts may not be a major concern should the coral be able to reinstate the more nutritionally advantageous symbiont as the dominant type during bleaching recovery. Finally, the rapid proliferation demonstrated by the heterologous Symbiodinium types and the associated metabolic cost to the host, could be an indication of the opportunistic nature of some of these types and may indicate a shift towards parasitism. It is imperative to extend this type of work to corals in the field to determine how these associations behave in nature. Also, in order to get a clearer picture of the diversity in symbiosis physiology, a wider range of Symbiodinium types needs to be investigated.</p>

The Influence of Symbiont Diversity on the Functional Biology of a Model Sea Anemone

<p>Cnidarian–dinoflagellate symbioses, particularly those between anthozoans and dinoflagellates of the genus Symbiodinium (commonly referred to as zooxanthellae) are widespread in the marine environment. They are responsible for the formation of coral reefs and are thus of great ecological importance. In recent years there has been an increase in the frequency and severity of episodes of coral bleaching resulting in degradation and mortality of coral reefs on a global scale. In order to gain a deeper understanding of how corals can adapt to changing environmental conditions, the effect that symbiont type has on the persistence and physiology of an association needs to be ascertained. The aim of this research was to determine how different symbiont types affect the nutritional biology and intracellular physiology of the symbiosis when in association with the sea anemone Aiptasia pulchella. The specific objectives of the study were to; (1) determine whether different symbiont types are equally as adept at supporting the energetic demands of the same host; (2) determine if internal pH (pHi) is a reflection of symbiont type and whether the optimal pH for photosynthesis coincides with the host cell pHi; and (3) test the influence of Symbiodinium type on host tissue glycerol and glucose pools. In order to answer these questions, aposymbiotic (i.e. symbiont-free) sea anemones were infected with different Symbiodinium types and the relationship between symbiont type, photosynthetic performance and autotrophic potential was tested. A range of ‘normal’ and novel cnidarian–dinoflagellate symbioses was also used to measure host cell pHi and to determine the optimal pHi of isolated intact symbiosomes (i.e. the vacuoles that house the symbionts), as well as to compare the amounts of free glycerol and glucose (metabolites) present in the host tissues. Different host-symbiont combinations were found to have different photosynthetic and respiratory attributes. Earlier onset of full autotrophy (i.e. when all metabolic carbon demands of the symbiosis were met by photosynthesis) and higher CZAR values (i.e. the contribution of zooxanthellae to animal respiration) were demonstrated by symbioses hosting Symbiodinium B1 both from the original (homologous) and different (heterologous) host. The study showed that Symbiodinium types differ in their pH optima and that the optimal pHi for photosynthesis does not always match the actual measured pHi. Symbiont type was also shown to have an effect on host tissue glycerol and glucose pools, with the associations harbouring the homologous Symbiodinium B1 attaining the highest concentrations of both metabolites. Findings from this study suggest that corals may be able to maintain an association with a range of Symbiodinium types, and hence potentially switch as a consequence of bleaching. The new symbiont type may not be as nutritionally advantageous as the original type however, which could have implications for the growth and survivorship of the coral, unless it is able to supplement its carbon demands heterotrophically. The rapid proliferation of some of the heterologous Symbiodinium types (e.g. Symbiodinium E2) inside the host indicates that, after bleaching, there is potential for fast symbiont establishment. The reduced carbon contribution of these heterologous symbionts may not be a major concern should the coral be able to reinstate the more nutritionally advantageous symbiont as the dominant type during bleaching recovery. Finally, the rapid proliferation demonstrated by the heterologous Symbiodinium types and the associated metabolic cost to the host, could be an indication of the opportunistic nature of some of these types and may indicate a shift towards parasitism. It is imperative to extend this type of work to corals in the field to determine how these associations behave in nature. Also, in order to get a clearer picture of the diversity in symbiosis physiology, a wider range of Symbiodinium types needs to be investigated.</p>

Species variability in the response to elevated temperature of select corals in north-western Philippines

Thermal stress events threaten coral populations by disrupting symbiosis between the coral animal and microalgal symbionts in its tissues. These symbionts are key players in the response of the coral holobiont to elevated temperature. However, little is known about the microalgal symbiont type in select corals in the north-western Philippines and how they contribute to the differential responses of coral species. Based on sequencing of major ITS2 bands from DGGE, the dominant algal symbiont inAcropora digitifera,A. millepora,A. tenuisandFavites colemaniwas identified to be closely related to ITS2 type C3u,Montipora digitatacontained ITS2 type C15, andSeriatopora caliendrumhosted ITS2 types similar to C3-Gulf and D1. Thin branching corals, such asA. tenuisandS. caliendrum, exhibited the greatest reduction in photochemical efficiency (Fv/Fm) and symbiont density at elevated temperature, followed byM. digitataandA. millepora, to a lesser extent.A. digitiferaandF. colemaniwere least affected by the temperature treatment. Reduction in Fv/Fm and symbiont density was more apparent inA. tenuisandA. milleporathan inM. digitataandF. colemani, although these species all host ITS2 type C3u symbionts. These results suggest that the impact of elevated temperature is influenced by factors apart from symbiont type. This highlights the importance of further studies on the diversity of corals and their microalgal symbionts in the region to gain insights into their potential resilience to recurring thermal stress events.

A complex symbiosis involving within species variation in the response ofDictyosteliumamoebae toBurkholderiabacteria

Recent symbioses, particularly facultative ones, are well suited for unravelling the evolutionary give and take between partners. Here we look at variation in wild-collected samples of the social amoebaDictyostelium discoideumand their relationships with bacterial symbionts,Burkholderia hayleyellaandBurkholderia agricolaris. Only about a third of field-collected amoebae carry a symbiont. We cured and cross-infectedD. discoideumhosts with different symbiont association histories and then compared the responses of the amoebae to each symbiont type. Before curing, field-collected clones did not vary significantly in overall fitness, but infected hosts produced morphologically different multicellular structures. After curing and re-infecting, host fitness declined overall. However, naturalB. hayleyellahosts suffered fewer fitness costs when re-infected withB. hayleyella,indicating that they have evolved mechanisms to tolerate their naturally acquired symbiont. Exploring relationships between endosymbionts and hosts that vary within species may also reveal much about disease dynamics.

Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis

The relationship between corals and dinoflagellates of the genusSymbiodiniumis fundamental to the functioning of coral ecosystems. It has been suggested that reef corals may adapt to climate change by changing their dominant symbiont type to a more thermally tolerant one, although the capacity for such a shift is potentially hindered by the compatibility of different host-symbiont pairings. Here we combined transcriptomic and metabolomic analyses to characterize the molecular, cellular, and physiological processes that underlie this compatibility, with a particular focus onSymbiodinium trenchii, an opportunistic, thermally tolerant symbiont that flourishes in coral tissues after bleaching events. Symbiont-free individuals of the sea anemoneExaiptasia pallida(commonly referred to as Aiptasia), an established model system for the study of the cnidarian-dinoflagellate symbiosis, were colonized with the “normal” (homologous) symbiontSymbiodinium minutumand the heterologousS. trenchii. Analysis of the host gene and metabolite expression profiles revealed that heterologous symbionts induced an expression pattern intermediate between the typical symbiotic state and the aposymbiotic state. Furthermore, integrated pathway analysis revealed that increased catabolism of fixed carbon stores, metabolic signaling, and immune processes occurred in response to the heterologous symbiont type. Our data suggest that both nutritional provisioning and the immune response induced by the foreign “invader” are important factors in determining the capacity of corals to adapt to climate change through the establishment of novel symbioses.