The ecophysiology of dimethylsulphoniopropionate (DMSP) in coral reef ecosystems : from cells to the community

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NO FULL TEXT AVAILABLE. This thesis contains 3rd party copyright material. ----- Australia is custodian of the world’s largest coral reef ecosystem, which is under increasing pressure from human activity and changes associated with a warming planet. Coral reef ecosystems are particularly sensitive to climate-induced changes to their physical environment, so despite their persistence over geological time, they are considered one of the most vulnerable of all marine ecosystems. The phenomenon of coral bleaching (the whitening of corals due to loss of their symbiotic algae Symbiodinium and/or their pigments) caused by unusually high sea temperatures, leads to devastating effects, which have been observed in reefs around the world. Today’s leading hypothesis into the cause of bleaching is that it results from accumulated oxidative stress on the thylakoid membranes of symbiont chloroplasts a result of damage to the photosynthetic machinery. Corals have mechanisms to supress the damaging effects of reactive oxygen species (ROS) using antioxidants and non-photochemical quenching (NPQ) for photoprotection. Recent research has shown that the sulphur compound, dimethylsulphoniopropionate (DMSP) and its breakdown products, which are produced by many microalgal species, including Symbiodinium, can act as an effective antioxidant to quench ROS. DMSP production by Symbiodinium is known to increase with elevated light and temperature, processes directly responsible for bleaching events, suggesting a possible role of DMSP in thermal stress responses. To investigate symbiont ROS and the possible antioxidant role of DMSP in corals, a model organism comprising cnidarian tissue and Symbiodinium algal cells (referred to as ‘coral explants’) was established. In Chapter 2, explant culturing methodology was optimised and explant physiology characterised to determine the suitability of explants for studying coral physiology. This work highlighted how these small, self-sustaining, skeleton-free models could be useful for investigations at the microscale, because they have comparable physiology and internal complexity to a parent coral. After validating their usefulness for studying tissue functions and processes, explants were used in Chapter 3 to investigate the interaction between ROS and DMSP at the cellular level, and confirm the applicability of explants for coral physiological and biochemical studies. Corals have some of the highest DMSP concentrations in the marine environment, suggesting that this molecule plays an important role in maintaining coral health. However, there are numerous proposed functions of DMSP in corals, including its role as an osmolyte and an antioxidant. Chapter 4 shows that under hyposaline conditions, there were species-specific differences in the use of DMSP by three common corals from the Indo-Pacific; Acropora millepora, Stylophora pistillata and Pocillopora damicornis. In this chapter, the increased ratio of dimethylsulphoxide to dimethylsulphoniopropionate (DMSO:DMSP) is suggestive of an antioxidant role, as DMSP and its breakdown products are oxidised to form DMSO, which can be further oxidised in the presence of ROS. By measuring the antioxidant activity in the host and the symbiont, the relative contributions of each component to hyposaline stress within the holobiont were determined, and it was shown that the life history strategy of the corals is an important factor determining whether a coral relies on the antioxidant function of DMSP or the enzymatic and non-enzymatic antioxidant systems. Under a changing climate, one of the driving factors of coral bleaching is increased sea-surface temperatures. In 2015-2017, the worst global coral bleaching event on record unfolded, it is therefore particularly important to understanding the bleaching response to predict how the diversity of coral reef ecosystems will change. In Chapter 5 fourteen common stress-response indicators comprising physiological, biochemical and molecular analyses were measured and four stages of bleaching were identified, which were conserved across two coral taxa. Species-specific differences were revealed in the bleaching response and the importance of the host in determining the sensitivity or tolerance to thermal stress was recognised. Additionally, Acropora millepora increased in intracellular concentrations of DMSP irrespective of symbiont loss under stress, highlighting the possible role of host DMSP production which could account for increased thermotolerance, as A. millepora survived 3 days longer than Stylophora pistillata under identical bleaching conditions. Another vital component of the coral holobiont is the coral-associated bacteria. Two main pathways are used by bacteria to metabolise DMSP: the cleavage pathway is significant because it result in the production of dimethylsulphide (DMS) which can diffuse into the atmosphere and can influence regional climate through increase cloud formation. The alternate pathway is through bacterial demethylation, resulting in acrylate and methanethiol (MeSH). Interestingly, it is not yet known which pathway is favoured under thermal stress, therefore in Chapter 6 DMSP-degrading bacteria in the coral and mucus of A. millepora were identified to elucidate the dominant pathway for DMSP degradation in warmer coral reef ecosystems. This thesis provides novel information about the antioxidant role of DMSP in reef-building corals. The interaction between DMSP and ROS across multiple scales was investigated: from the cellular level up to the entire coral holobiont using physiological, biochemical and molecular approaches and delivers new information on the species-specific differences in DMSP concentration and how this influences species tolerance to environmental stress. These results provide a comprehensive study using a wide range of bleaching response indicators, and show for the first time the DMSP antioxidant function of DMSP is conserved from the micro to macro scale, highlighting the importance of DMSP in coral reef ecophysiology.
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