Understanding the Molecular and Physiological Responses of Tropical Coralline Algae to a Changing Ocean

Abstract

Coral reefs are amongst the most biologically diverse ecosystems on our planet, supporting the livelihoods of millions of people globally. Despite their economic and ecological importance, human-driven global change is posing a major threat to the integrity of coral reefs worldwide. Ocean warming (OW) and ocean acidification (OA), both brought on by increased atmospheric CO2, are adversely affecting coral reefs and the organisms that inhabit them, particularly those organisms that calcify. Crustose coralline algae (CCA) are calcifying red macroalgae that provide essential ecosystem functions to coral reefs worldwide. CCA help to build and stabilise the coral reef framework and contribute to reef resilience and recovery by inducing the settlement of coral larvae to the reef. Previous research has shown CCA to be vulnerable to OW and OA, with resulting changes to their physiology and biology (i.e., reductions in calcification, abundance, survival). However, research on CCA lags behind other coral reef organisms, particularly in terms of their acclimatisation potential and knowledge of molecular, cellular, and metabolic processes. Given the known vulnerability of CCA, urgent research is required to understand how CCA will respond across molecular and physiological levels to global change drivers and this could directly aid in reef restoration efforts. The first data chapter of my thesis (Chapter 2) provides previously missing molecular information for CCA. De novo transcriptomes were compiled for four species, Porolithon cf. onkodes, Sporolithon cf. durum, Lithophyllum cf. insipidum, and Lithothamnion proliferum, that commonly occur in Australia’s Great Barrier Reef (GBR). Analyses of orthologous genes were conducted between CCA species and two noncalcifiying red algae, Chondrus crispus and Gracilariopsis chorda. Functional enrichment analysis of CCA orthologous proteins revealed a higher-than-expected number of sequences in categories relating to regulation of biological and cellular processes, such as actin related proteins, heat shock proteins, and adhesion proteins. This study allowed me to create reference transcriptomes that can be used in future studies investigating molecular responses of CCA to OW and OA and offered insight into the evolution of coralline algae. In Chapter 3 I investigated the differential physiological and transcriptomic responses of two species of CCA, P. cf. onkodes and S. cf. durum, to global change drivers (OW and OA). Previous literature investigating the responses of CCA species to global change drivers found variable results and these have been largely speciesspecific. The two species used in this study have been documented to have contrasting responses to OW and OA. Species-specific responses were seen in both the metabolic rate measurements and in the number of differentially expressed genes (DEGs) detected, indicating resilience in one species and not in the other. This study was also the first to reveal pathways and proteins that are differentially regulated in response to global change drivers. This work will help to predict the fate and functioning of different CCA species in future ocean conditions. Early life history stages of organisms are thought to be more impacted by climatic stressors than their adult stages, therefore, I investigated the responses across different life history stages of the CCA species S. cf. durum to varying levels of temperature and pCO2 (Chapter 4). In this study, I used adults and germlings of their first generation (F1). The findings suggest that adult stages of S. cf. durum are largely robust to end of century levels of temperature and pH, in terms of their survival and metabolic rates, and indicate that adult stages may be able to acclimatise to global change. On the other hand, the data show early life history stages of this species are highly sensitive to global change stressors with reductions in their survival and growth. This could impact the persistence of this species in future oceans. How an acclimation history to predicted, future levels of temperature and/or pH affects the physiological responses to chronic and acute thermal stress was investigated in the last chapter of my thesis (Chapter 5). P. cf. onkodes was acclimated to chronic, varying levels of temperature and pH for 6 weeks and then subjected to an acute, increasing temperature experiment (+ 4 – 6 oC). The findings from this study suggest that an acclimation history to elevated temperature will reduce the thermal tolerance of P. cf. onkodes to withstand anomalous temperature events, which are projected to increase in number and severity within this century. Overall, the findings of the work described in this thesis have: 1) Made available the first comprehensive and annotated de novo transcriptomes for any species of CCA; 2) shown that physiological and transcriptomic response to global change drivers is species specific, with some CCA being more resilient and others not, and identified proteins relating to physiological processes that are differentially expressed in response to stress; 3) supported the hypothesis that early life history stages of CCA will be more impacted by global change drivers than adults of the same species, with possible plasticity being seen in adults in response to sustained exposure to stress; and 4) determined an acclimation history of elevated temperature will reduce thermal tolerance and productivity in CCA. My thesis also provides evidence that more anciently diverged genera (e.g., Sporolithon) are physiologically more robust and molecularly less responsive to global change drivers. My thesis demonstrates the strength of incorporating molecular, life history stage, and acclimation type approaches to more holistically understand the future of a critical group of reef-building organisms under global climate change and will ultimately contribute to conservation efforts that are currently being made into saving coral reefs worldwide.