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Symbiotic COOperation and Boring Activity of Cliona sponges under a climate change context

Periodic Reporting for period 2 - SCOOBA (Symbiotic COOperation and Boring Activity of Cliona sponges under a climate change context)

Reporting period: 2019-03-01 to 2020-02-29

Rising atmospheric CO2 concentrations are changing the chemistry of the oceans. Specifically, seawater pH is in decline – a process known as ocean acidification (OA). Coral reefs are particularly susceptible to OA. The carbonate structures comprising reefs are built by corals, but OA threatens to weaken and erode calcareous reefs. Another key element in reef dissolution, bioerosion (i.e. the process of sponge growth into calcareous structures causing reef degradation) may increase under future ocean conditions, particularly as a result of warming. The major bioeroding organisms on reefs are sponges belonging to the genus Cliona. Future environmental conditions may shift coral reefs to a state of perpetual decline. It is essential that we understand the role sponges play in that process. The most aggressive bioeroding sponges are those that harbor algal symbionts belonging to the same group found in corals (i.e. Symbiodinium). In corals, the algal symbionts provide the nutrition they need to precipitate calcium carbonate and form large reef structures. In sponges, the energy is used to increase rates of bioerosion. In addition to the interaction with Symbiodinium, most of the sponges host a wide range of bacteria, which are crucial to the sponge behavior.

The combination of ocean warming with ocean acidification causes that corals (and other calcifying organisms in temperate regions) are undergoing a significant decline worldwide, however, bioeroding sponges may have an ecological advantage under future conditions. This might have dramatic consequences because reefs support 25% of marine life. The impact would be not only in terms of food resources obtained from the sea but also tourism would be severely affected. The economic impact is valued in $3.4 billion only in the USA. So, the focus on bioeroding sponges is especially important given how ocean acidification may accelerate the rate of boring into calcium carbonate structures by these type of sponges.

The scientific aim of this project is to study how symbionts interact with each other and with their host in terms of the sponge performance under a climate change context. We characterize the symbiotic community associated to clionaid sponges from tropical habitats and determine the effect of future environmental conditions on sponge bioerosion from multiple perspectives, estimating bioeroding activity and assessing expression of potential genes related to this process.

The main conclusions of the project are (i) clionaid sponges show a species-specific core microbiome with dominant OTUs partly shared among species but with species-specific enrichments; (ii) Symbiodinium populations of Cliona varians was diminished due to an exposure to high temperatures; (iii) temperature also shrank alpha and beta diversities of sponge microbiome; (iv) high bioerosion was observed at high temperature and mid pH conditions. While symbiotic dinoflagellates are reduced at high temperatures, the bioeroding activity is increased. So, bioerosion might be favoured by other mechanisms that need to be further studied. We expect that differential gene expression will shed light on how bioeroding sponges perform under a climate change context.
In the first year of the project, we published a chapter entitled Molecular and Functional Ecology of Sponges and Their Microbial Symbionts (Hill and Sacristán-Soriano 2017) in the book Climate Change, Ocean Acidification and Sponges, published by Springer Nature, addressing the importance of sponge-microbe symbiotic interactions for marine ecosystems.

For the study of sponge-associated microbial communities, we developed a standardized methodology and analytical pipeline, which is described in the publication Sacristán-Soriano et al. (2019).

There are four different bioeroding sponges in the subtropical region we studied (Florida Keys, FL USA). We characterized and compared the microbial consortia associated with those species to analyze their specificity and plasticity within hosts and over a spatial scale. These clionaid sponges presented species-specific core enrichments (Sacristán-Soriano et al. status: minor revision)

We also applied the developed standardized methodology and analytical pipeline to study sponge-associated microbial communities from polar environments. This study reveals that sponge-associated prokaryote communities are consistently detected within a particular sponge species regardless of the collection site (Sacristán-Soriano et al. status: under review).

We focused on the highly abundant sponge Cliona varians, which was cultivated under different environmental conditions (Figures Close view sponge and Experiment setup). We observed high bioerosion at high temperature and mid pH conditions (7.8) measured as block weight change and in terms of expelled chip density (Figures Sponge chip SEM1,SEM2, and SEM3). The Symbiodinium population of Cliona varians was diminished due to an exposure to high temperatures. When we observed the sponge microbiome, there was a clear difference in alpha and beta diversity among sampling points and between temperatures.

Results of SCOOBA will be exploitable by using them in further internal research activities and to establish new research collaborations. Results are not expected to be protected due to a lack of potential for commercial or industrial exploitation.
The original idea of the project was to use sponge cell aggregates to test current and future climate projections on the sponge development and performance. However, the difficulty of obtaining viable cell aggregates forced us to change our workplan and we decided to use small sponge fragments to accomplish our goals (Figure Sponge clones).

During the third year, we determined the potential effect of climate change on the sponge performance and its bioeroding activity from different perspectives. At the end, we could gain insights into how sponges regulate these environmental stressors at a genetic level and see how the symbiotic community is affected by climate perturbations.

We foresee mid-term and long-term impacts coming out of this project. Once we know in detail how ocean acidification and ocean warming affect the bioerosion of these sponges into calcareous structures build by corals and determine the genetic regulation by the sponge under this perturbation, we could anticipate the fate of coral reefs and could have the knowledge of how the eroding activity is regulated. So, we could provide the scientific bases for a good management and protection of coral reefs and other environments where boring sponges are abundant. We could also suggest detailed actions for the conservation of these marine ecosystems and get politicians involved in developing a new protection policy. Although coral reefs cover around 1% of the ocean floor, they support 25% of marine life. Degradation of these habitats means that local marine food resources are threatened but also tourism would be severely affected. So, the economic impact could be enormous (billions of euros).

The wider societal implications of the project will be fundamentally to increase the awareness of the society towards the consequences of climate change in the marine life using an emblematic system, the coral reefs. We will also point out the knock-on effect on socio-economic issues, and give tips about how a person as individual can contribute to diminish the effects of global warming.
Close view sponge fragment
Experiment setup
Sponge clones
Sponge chip SEM1
Sponge chip SEM2
Sponge chip SEM3