Manipulation of coral photosymbionts for enhancing resilience to environmental change

Chakravarti, Leela J. (2019) Manipulation of coral photosymbionts for enhancing resilience to environmental change. PhD thesis, James Cook University.

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Ocean warming is occurring at an unprecedented rate. Only a small increase in seawater temperature can disrupt the symbiotic relationship between corals and their photosynthetic algae causing coral bleaching. The bleaching threshold of corals is largely dependent on the microalgae they host. Some studies have indicated the ability for small increases in corals' tolerance to environmental change through shifts in their symbiont communities. However, the increase in frequency of severe bleaching events that have led to worldwide loss of coral cover indicate that this is not enough for coral persistence. This thesis investigates the feasibility and efficacy of manipulating algal symbiont populations associated with corals to enhance their stress tolerance in an era of rapid environmental change.

Due to their comparatively short generation time, coral algal symbionts have the potential to evolve more rapidly to environmental changes than their coral host. Chapter two investigates the thermal tolerance of the most common algal symbiont of Great Barrier Reef corals, Cladocopium goreaui, after ~80 asexual generations (2.5 years) of in vitro directed laboratory evolution at an elevated temperature. Using a reciprocal transplant design, I show that the upper temperature tolerance range of the selected C. goreaui increased, evidenced by superior photophysiological performance, growth rates and lower levels of extracellular reactive oxygen species, relative to wild-type cells. In comparison, wild-type C. goreaui cells were unable to photosynthesise or grow at elevated temperature. The enhanced thermal tolerance of the selected C. goreaui in hospite was less apparent. Two of three coral species tested showed positive growth when harbouring the selected C. goreaui at elevated temperature, compared to those that hosted the wild-type cells that had negative growth at elevated temperature. Despite this, recruits of the three coral species bleached regardless of whether they hosted the thermally selected or the wild-type C. goreaui.

Important next steps were to decipher the genetic basis underlying enhanced thermal tolerance in the selected algal C. goreaui. Therefore, Chapter three investigates the differences in gene expression between the wild-type and selected cells during the reciprocal transplant experiment. Samples were taken at three time points over 35 days and a de novo transcriptome was assembled. Comparative transcriptomics revealed significant differences in gene expression between the wild-type and selected C. goreaui at elevated temperature. The wild type cells displayed an unstable transcriptomic response of upregulated genes over time, involving large changes in the numbers of genes upregulated and their associated functions. Down-regulated genes, however, were consistently photosynthesis-related, concurrent with their inferior photosynthetic performance at elevated temperature as detailed in chapter 2. The thermally selected C. goreaui shared very few differentially expressed genes with the wild-type cells, having a more stable transcriptomic response to elevated temperature over time. Upregulated genes largely involved those encoding DNA transcription and initiation processes. Although some photosynthetic-related genes were downregulated during one time point, the majority of downregulated genes were involved in the regulation of cell projection organisation.

Chapters two and three investigate the most common Great Barrier Reef species of coral photosymbiont, C. goreaui. However, the family that they belong to, the Symbiodiniaceae, is genetically diverse and studies have found wide phenotypic differences between species, with differing thermal tolerances. This led me to testing whether thermal selection experiments could be used successfully across a range of species in the Symbiodiniaceae. Therefore, in chapter four I examine the response of five genetically distinct strains of the Symbiodiniaceae, belonging to four genera, over the course of approximately one year. For three genera I observed a stable adaptive change after only 41-69 asexual generations, where selected cells grew faster and in some cases had higher photosynthetic efficiencies than their wild-type counterparts at elevated temperature. The observed increases in growth rates are comparable with evolutionary experiments in other microalgae, where thermally selected populations have been exposed to elevated temperatures for up to 400 generations.

The Symbiodiniaceae are not the only algae to be associated with corals. Apicomplexan-like microalgae were discovered in 2008 and the phylum Chromerida was created. Chromerids have been isolated from corals and contain a functional photosynthetic plastid. Their discovery opens a new avenue of research into the use of alternative/additional photosymbionts of corals. Furthermore, not only do global environmental changes pose a threat to marine organisms but also the simultaneous effects of local stressors such as herbicide additions to coastal systems that often coincide with high summer temperatures. Diuron is one of the most commonly applied herbicides in the catchments of the Great Barrier Reef, acts to inhibit photosynthesis in plants and algae and has been directly linked to coral bleaching. In chapter 5 I test the performance of four chromerid populations as well as C. goreaui in response to elevated temperature, diuron and their combined exposure. Three of the four chromerid strains exhibited high thermal tolerances and two exceptional herbicide tolerances, greater than any observed for photosynthetic microalgae. I subsequently investigate the ability of the chromerids to form a symbiosis with larvae of two common GBR coral species under ambient and stress conditions. Chromerid uptake by coral larvae was low compared to C. goreaui. I did not observe any overall negative or positive larval fitness effects of the infection with chromerid algae vs. C. goreaui. However, the possibility that chromerid algae may have more important roles in later coral life stages or with other species of coral cannot be excluded.

The research presented in this thesis is among the first to test the possibility of experimental evolution to enhance the thermal tolerance of coral symbionts belonging to the Symbiodiniaceae, as well as the use of the potentially alternative symbionts, the chromerids. My results show that it is possible to experimentally evolve cultured Symbiodiniaceae strains across multiple species and highlight the genetic and molecular pathways that underpin thermal tolerance in the most common Great Barrier Reef species, C. goreaui. Despite increased thermal tolerance of the thermally-selected Symbiodiniaceae in vitro and the high thermal and diuron tolerance of some chromerid populations, these were unable to significantly enhance the upper thermal limit or diuron tolerance of the coral-algal symbiosis. Therefore, further work into the algal-coral association and bleaching response is required to assess whether algal symbiont manipulation has the potential to be a valuable tool in coral reef conservation and restoration initiatives in a rapidly changing ocean.

Item ID: 64541
Item Type: Thesis (PhD)
Keywords: acclimation, Acropora cytherea, Acropora hyacinthus, Acropora sarmentosa, Acropora, adaptation, assisted evolution, Chromera velia, Cladocopium goreaui, climate change, coral bleaching, diuron, experimental evolution, Great Barrier Reef, ocean warming, Symbiodiniaceae, Symbiodinium, Symbiosis, thermal stress, Vitrella brassicaformis
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Copyright Information: Copyright © 2019 Leela J. Chakravarti.
Additional Information:

Three publications arising from this thesis are stored in ResearchOnline@JCU, at the time of processing. Please see the Related URLs. The publications are:

Chapter 2: Chakravarti, Leela J., Beltran, Victor H., and van Oppen, Madeleine J.H. (2017) Rapid thermal adaptation in photosymbionts of reef-building corals. Global Change Biology, 23 (11). pp. 4675-4688.

Chapter 4: Chakravarti, Leela J., and van Oppen, Madeleine J.H. (2018) Experimental evolution in coral photosymbionts as a tool to increase thermal tolerance. Frontiers in Marine Science, 5. 227.

Chapter 5: Chakravarti, Leela J., Negri, Andrew P., and van Oppen, Madeleine J.H. (2019) Thermal and herbicide tolerances of chromerid algae and their ability to form a symbiosis with corals. Frontiers In Microbiology, 10. 173.

Date Deposited: 07 Oct 2020 04:10
FoR Codes: 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060303 Biological Adaptation @ 33%
05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050101 Ecological Impacts of Climate Change @ 34%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 33%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 100%
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