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NEWSLETTER ISSUE No. 4 | JULY 2018 www.rsrc.kaust.edu.sa

Contents Page 3

Heat-resistant corals in the Middle East could save the world’s dying reefs

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Anemones take the heat with a little help from their friends

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Coral tricks for adapting to ocean acidification

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Remote corals pay the price of climate change

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From Germany to Saudi Arabia: A journey for Isabelle

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RSRC publication featured in BBC News

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Mysterious gentle giants gather off Saudi coast

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Italian Red Sea Research Event In Jeddah

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Roberto Arrigoni has been awarded with the international prize “Benazzi Lentati”

Message from the Director Welcome to our newsletter! As of July 1st, the RSRC has launched a new series of projects with our Center Applied Research Funds (CARF). Across KAUST, research centers are expected to apply their CARF funding towards projects with anticipated value beyond scientific knowledge. For the RSRC, one major area of focus is in the coral reef ecosystems of the Red Sea. In particular, it will be important for the Kingdom to understand how Red Sea reef systems are impacted by stress events and to know how reef systems can recover after disturbances. This month’s newsletter accordingly features some of the recent highlights of reef-related work conducted within the RSRC. Next month, we will begin welcoming a new cohort of students and kicking off a new academic year. I hope you will join me in welcoming some new faces in the Center soon! Michael Berumen Acting Director of KAUST Red Sea Research Center Professor of Marine Science

Message from the Director | 2

Heat-resistant corals in the Middle East could save the world’s dying reefs Prof. Michael Berumen’s interview for CNN Travel By Sarah Lazarus, CNN (CNN) Coral reefs are in crisis. Around the world, they are being wiped out by rising sea temperatures -- a consequence of climate change. But in one region, some corals are withstanding the heat. Off the coast of the Arabian Peninsula, there are pockets of resistance. Consequently, this area has become a hotbed for research as marine biologists try to figure out what gives these corals their ability to survive warming seas and whether genetic technology could -- and should -- be used to save dying coral reefs, before we lose them forever.

Back from the brink Researchers at Saudi Arabia’s King Abdullah University of Science and Technology (KAUST) are using genetic analyses to decipher why Red Sea corals are much less prone -- although not immune -- to bleaching, than the exact same species living on the Great Barrier Reef. They are also comparing individual corals to determine why some show more heat tolerance than others. Once key lifesaving genes have been identified, the next step will be to breed the corals that carry them. “The question is: If we can identify the ‘supermom’ and ‘superdad’ corals, can we create ‘superbabies’ that will be more resilient to stressful conditions?” says Michael Berumen, who leads KAUST’s Red Sea Research Center.

Ethical dilemmas Most marine biologists say that experimental measures being tested in the lab should not be deployed in the wild unless absolutely necessary and, even then, with extreme caution. “Some scholars have talked about human-assisted migration -- moving heat-resistant corals from the southern Persian Gulf to other parts of the world,” says John Burt, a marine biologist at NYU Abu Dhabi, in the United Arab Emirates, “but we don’t know the genetic implications, and there’s a risk of introducing disease and parasites.” And as with any genetic engineering technology, the application of breeding research could lead to unexpected pitfalls. “Our remit as scientists is to say which options are on the table,” says Berumen. “The real dilemma comes later in the form of the ethical question: Should we use these technologies or not?” He adds that good quality data that quantifies the pros and cons is key to decision making. Ultimately, though, “it is up to reef management authorities to decide what to do within their jurisdictions.” There is consensus among coral experts that we should do more to preserve the reefs we already have, rather than relying on a scientific fix. At the moment, Berumen says he’s not ruling anything out. “The situation is critical in some parts of the world and large areas of coral reef have been killed by climate change stress, so extreme options might need to be on the table.”

The KAUST scientists are also examining the corals’ microbiomes -- the bacteria, viruses and fungi that live in association with them. “Each individual coral may have up to a thousand types of bacteria living on or inside it. We don’t yet know how important a role they play in heat resilience, but we assume it’s significant,” says Berumen.

Read more here. Research Highlights | 4

Coral tricks for adapting to ocean acidification A molecular process that signals distress could also help corals adapt to climate change.

We hope our contribution will change the current perception among reef biologists that epigenetics do not contribute much to coral resilience.” - Dr. Yi Jin Liew RSRC former postdoc

A process that changes the regulation of genes could help corals acclimatize to the impacts of global warming. Cells commonly control gene expression by adding a methyl group to part of the DNA, changing how the information on the DNA is read without changing its genetic code. Researchers at KAUST wanted to investigate whether DNA methylation could play a role in helping corals adapt to climate change. They placed colonies of the smooth cauliflower coral, Stylophora pistillata, in seawater aquariums with varying acidity levels for two years. Ocean acidification is a consequence of climate change and hinders the ability of corals to produce the calcium carbonate skeleton they need to maintain their structures. The researchers hypothesized that DNA methylation might allow corals to mitigate these effects by changing the way they grow. After two years, the team sequenced the genomes of the corals and determined changes in methylation patterns.

5 | Research Highlights

“We noticed that corals grown under more acidic conditions had higher levels of DNA methylation,” says geneticist Yi Jin Liew. “Genes with increased methylation were related to cell growth and stress response, but not to calcification as we initially proposed,” he says. In line with this finding, the team discovered that cell and polyp sizes in the corals also increased with rising acidity. “The coral polyps sit in little cavities called calyxes into which they can retreat for protection,” explains molecular biologist Manuel Aranda. Larger polyps have larger calyxes. “If the calyx is bigger, the coral needs to produce less skeleton to grow at the same pace. I call this the ‘Swiss cheese hypothesis,’ where the coral makes bigger holes so it needs to make less cheese, which allows it to grow at the same speed even though skeletal production is impaired.” This trait would be advantageous in an environment where competition for space and light is an important selective pressure.

“We hope our contribution will change the current perception among reef biologists that epigenetics do not contribute much to coral resilience,” says Liew. The team next plans to investigate whether these epigenetic changes can be passed down to future generations. “The idea is fairly revolutionary,” says Liew.

Related publication Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral Liew, Y.J. Zoccola, D., Li, Y., Tambutté, E., Venn, A.A., Michell, C.T. Cui, G., Deutekom, E.S., Kaandorp, J.A., Voolstra, C.R., Forêt, S., Allemand, D., Tambutté, S. & Aranda, M Science Advances Vol. 4, no. 6, eaar8028

The findings indicate that DNA methylation can be used as a marker of coral stress. This epigenetic mechanism might also be harnessed to grow corals under future ocean conditions to prime them for increased temperatures before placing them on reefs, says Aranda. This process is known as environmental hardening. Read this story and more on KAUST Discovery here. Research Highlights | 6

Remote corals pay the price of climate change Corals, even in the most far-flung locations, are being affected by climate change but fare better in marine protected areas. The coral reefs of a Samoan island in the remote southwest Pacific are in a surprisingly poor condition, highlighting the far-reaching impacts of climate change. KAUST marine scientists joined colleagues on the research schooner Tara to examine the impacts of climate change on coral reefs surrounding Upolu, an island just 74 kilometers long and 24 kilometers wide, home to about 135,000 Samoans. Small island populations largely rely on healthy coral reef systems for their livelihoods, but the status of these reefs in remote parts of the world is poorly documented. “Investigating coral reefs in remote locations can teach us about global and local impacts on these ecosystems,” says molecular biologist Maren Ziegler. Maren is a former postdoc from Associate Professor Christian Voolstra’s lab who has now moved on to a position at Justus Liebig University Giessen in Germany as a junior research group leader.

Read the full story on KAUST Discovery here

Ziegler was chief scientist on board the Tara Pacific Expedition toward the end of 2016 when researchers surveyed 124 sites over 83 kilometers of Upolu’s coastal coral reefs. “Despite the distance from large urban centers, live coral cover was extremely low,” says Ziegler. Live coral covered less than one percent of half the sites surveyed and below 10 percent at 78 percent of the study sites on the reefs. “This means that climate change, and in particular global warming, is probably affecting coral reefs everywhere on our planet now, even around small island states in the Pacific that are only contributing a very small fraction of the global greenhouse gas emissions.” Two of the reef fish species known to live in the area were 10 percent smaller off Upolu than at neighboring islands. They swam in small schools of just five fish, yet they were commonly found in schools of 20 to 60 off other Pacific islands. These observations suggest that the fish habitat is degraded and that heavy fishing is affecting the coastal ecosystem around Upolu.

KAUST’s Maren Ziegler (center), who was chief scientist on board for the Samoan leg of the expedition, and her colleagues surveyed 124 sites over 83 kilometers of Upolu’s coast. © Pierre de Parscau, Tara Pacific Expedition 20162018 A degraded reef in Samoa (left) shows that even reefs far from large urban centers are being affected by climate change. However, healthy reefs (right) were found within Upolu’s marine protected areas and near the Cook Islands southwest of Samoa, indicating that local action to protect resources can go a long way. © Gaelle Quéré ,Tara Pacific Expedition 2016-2018

7 | Research Highlights

From Germany to Saudi Arabia: A journey for Isabelle Article by David Murphy KAUST News

Thanks to her globetrotting family, KAUST former postdoctoral fellow Isabelle Schulz’s earliest journey came at five months old, when her German parents, Manfred and Doris, moved from Switzerland to Riyadh, Saudi Arabia. Manfred worked as a salesman for the automation company Asea Brown Boveri, selling turbine engines to a multitude of clients across the region. Three years later, Isabelle, her two siblings and her parents moved again, this time to Algeria for her father’s work. Isabelle spent her formative years there, where she had the almost infinite sand dunes of the country as her backyard and playground. In Algeria, she also discovered her two passions: marine science and travel. Many years later in the northwestern German town of Meerbusch, a newly graduated Isabelle began planning her next move after completing her Ph.D. in marine biology at the Alfred Wegener Institute for Polar and Marine Research (AWI) in Bremerhaven, Germany. Her thoughts drifted back to her childhood in North Africa and her youth spent exploring the Middle East. Isabelle was keen to live abroad again, and thanks to a discussion with an AWI alumni friend, her newest adventure took shape. “It was Xabier Irigoien, the former director of the RSRC, who gave me the opportunity to join KAUST in 2014, and when he left, I started working for Professor Carlos Duarte and Professor Susana Agusti on various projects. I am very grateful to Xabier, Carlos and Susana for all these opportunities,” she added. Read the full story here.

Isabelle Schulz, a former postdoc in the RSRC, and her parents Doris and Manfred Schulz. Doris and Manfred traveled by car from Germany to Saudi Arabia to visit Isabelle at KAUST. © 2018 Lilit Hovhannisyan

Returning to the Kingdom In May 2017, Manfred and Doris sat down at their kitchen table in Meerbusch to plan their next trip abroad—this time a road trip to visit Isabelle at KAUST. What would seem a daunting trip to people half their age barely registered with the adventurous couple, who, in their 50 years of marriage, have already traveled through 90 countries—they’ve driven the Silk Road from Germany to China; driven the length of the Americas; traveled the length and breadth of Asia; and taken regular forays in Europe, North Africa and the Middle East. “From when we first met, my wife and I were always abroad—we were used to the road from an early age,” Manfred noted. Their trip was roughly divided into two legs; the first leg would take them from Meerbusch to Passau, a German city on the Austrian border; into eastern Croatia via Slavonski Brod; and then through Serbia’s third largest city, Niš; before continuing south to Turkey. They traversed Turkey in four days from Edirne in the country’s northwest region through to its easternmost district, Doğubayazıt. The second leg took them through the Middle East to Dubai and through the United Arab Emirates and onto Riyadh. In Riyadh, the Schulz couple pulled up in their Land Cruiser for a brief respite before driving the width of the vast expanse of the Arabian Peninsula to reach KAUST on April 11—a mere 21 days after they left their home in Germany. They drove the 963 kilometers from Riyadh to Jeddah in one day. Recent News | 8

RSRC publication featured in BBC News Heatwaves ‘cook’ Great Barrier Reef corals Article by Mary Halton, Science Reporter, BBC News

Prolonged ocean warming events, known as marine heatwaves, take a significant toll on the complex ecosystem of the Great Barrier Reef. This is according to a new study on the impacts of the 2016 marine heatwave, published in Nature. In surveying the 3,863 individual reefs that make up the system off Australia’s north-east coast, scientists found that 29% of communities were affected. In some cases up to 90% of coral died, in a process known as bleaching. This occurs when the stress of elevated temperatures causes a breakdown of the coral’s symbiotic relationship with its algae, which provide the coral with energy to survive, and give the reef its distinctive colors. Certain coral species are more susceptible to this heat-induced stress, and the 2016 marine heatwave saw the death of many tabular and staghorn corals, which are a key part of the reef’s structure. Researchers led by Terry Hughes at Australia’s ARC Centre of Excellence for Coral Reef Studies looked at aerial observations of the entire 2,300km reef between March and November 2016. These were combined with underwater surveys at over 100 locations.

Healing time Not all areas of the reef, or all coral species, were equally affected. Some were better able to tolerate the stressful conditions, or to bounce back afterwards. In the much warmer waters of the Red Sea, researchers at King Abdullah University of Science and Technology in Saudi Arabia have been looking at how corals can potentially adapt to increased temperatures. Their results, published in the Proceedings of the Royal Society, indicate that it is the partner algae, and not the coral themselves, who may be responsible for a capacity to tolerate heat stress. With year-round temperatures of 29 - 30C, the Red Sea is a more thermally stable environment than many other reef communities. The Symbiodinium algae there have adapted to tolerate the warmest ocean waters in the world, and it appears this may also make them more resilient to the stresses of changing temperatures. Partnering up with these particular algae could give corals an advantage.

“We saw some corals rapidly dying,” explained Dr. Scott Heron, another of the study’s authors. “Bleaching... is essentially a starvation process that occurs over one to two months. This rapid onset is not the same starvation mechanism. The best way to describe it is akin to cooking,” added the NOAA Coral Reef Watch scientist. They found that these “cooked” corals were dying within two to three weeks. The northern section of the reef, some 700km long, was worst affected, with 50% of the coral cover in the reef’s shallowest areas being lost within eight months. 9 | Recent News

It’s not yet clear what this could mean for other reef environments in danger of bleaching, but lead author Maha Cziesielski says that swapping to a different algae species is something corals already do in nature: “It’s quite common... it’s called symbiont shuffling. Association with more ‘thermotolerant’ algae can play a very important role in adapting to warmer environments,” she told BBC News. She cautions that there will be no silver bullet when it comes to stalling the impact of climate change on reef environments. “We don’t understand the reef system well enough yet to have one answer... I don’t think we have a large scale solution for this yet. [But this is] work that can in the future lead to something bigger.”

Read the full article here.

Related publication: Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts M. J. Cziesielski, Y. J. Liew, G. Cui, S. Schmidt-Roach, S. Campana, C. Marondedze, M. Aranda Proc. R. Soc. B. 285 : 20172654

Annual average temperature profiles of sampling locations of the three investigated Aiptasia strains originating from North Carolina (Wilmington), Hawaii (Ka¯ne’ohe Bay) and the Red Sea (Al Lith). The average monthly temperature is denoted by a solid line. Shading around lines represent maximum and minimum temperature (temperature data taken for closest location to sampling area from www.seatemperature.org).

Abstract Corals and their endosymbiotic dinoflagellates of the genus Symbiodinium have a fragile relationship that breaks down under heat stress, an event known as bleaching. However, many coral species have adapted to high temperature environments such as the Red Sea (RS). To investigate mechanisms underlying temperature adaptation in zooxanthellate cnidarians we compared transcriptome- and proteome-wide heat stress response (24 h at 32°C) of three strains of the model organism Aiptasia pallida from regions with differing temperature profiles; North Carolina (CC7), Hawaii (H2) and the RS. Correlations between transcript and protein levels were generally low but inter-strain comparisons highlighted a common core cnidarian response to heat stress, including protein folding and oxidative stress pathways. RS anemones showed the strongest increase in antioxidant gene expression and exhibited significantly lower reactive oxygen species (ROS) levels in hospite. However, comparisons of antioxidant gene and protein expression between strains did not show strong differences, indicating similar antioxidant capacity across the strains. Subsequent analysis of ROS production in isolated symbionts confirmed that the observed differences of ROS levels in hospite were symbiont-driven. Our findings indicate that RS anemones do not show increased antioxidant capacity but may have adapted to higher temperatures through association with more thermally tolerant symbionts.

Recent News | 10

Mysterious gentle giants gather off Saudi coast

The team, led by oceanographer Burton Jones with marine zoologist Stein Kaartvedt from the University of Oslo placed echosounders on the seabed close to coral reefs where the whale sharks are known to aggregate.

Investigations of prey patterns fail to explain why whale sharks aggregate off the coast of Saudi Arabia.

Echosounders send sound pulses into the water, which bounce back as echoes when they hit very small objects, like fish, plankton, sediment or even air bubbles, Hozumi explains. Sound echoes bounce back at different strengths, depending on what they strike, enabling researchers to differentiate between different kinds of small matter in the water.

The availability of tiny prey near a coral reef in the eastern Red Sea seems not to be the reason that whale sharks aggregate there every spring. In recent years, juvenile whale sharks have been discovered gathering at a coral reef, 4 kilometers off the coast of Saudi Arabia between February and May. This provides the opportunity for scientists at KAUST’s Red Sea Research Center to study their behaviors. “Whale sharks are under threat from targeted fisheries and as bycatch and are listed as endangered by the IUCN Red List,” says RSRC former Ph.D. student Aya Hozumi. “However, we have limited understanding of their ecology and life history, which poses a challenge to conservation efforts.” Whale sharks, with lengths surpassing 12 meters, are the largest fish in the world. They feed by opening their mouths to filter the water for tiny fish and floating organisms called zooplankton. Hozumi and her colleagues wanted to investigate whether gatherings of whale sharks each spring near Al-Lith, Saudi Arabia, were due to rising levels of the zooplankton prey during the same season. Read more on KAUST Discovery here. 11 | Research Highlights

The team was surprised to find that the layer of tiny marine organisms in the area did not peak during the whale shark’s spring season near Al-Lith. Instead, the levels of organisms in the study area were generally steady before, during and after whale shark season.

Italian Red Sea research event in Jeddah On May 14, Professor Daniele Daffonchio of KAUST Biological and Environmental Science and Engineering Division and the Red Sea Research Center presented his research alongside Professors from two Italian universities at the Italian Cultural Centre in Jeddah to a diverse local and international audience. The presentation of their research was complemented by an immersive multimedia exhibition combining underwater film and photography focusing on the biodiversity found within the Red Sea. Entitled “water.colors: a Red Sea biodiversity exhibition”, the collection was organized and curated by KAUST ARTmosphere curator, Solkem N’Gangbet. The event, introduced by the Consul General of Italy, Elisabetta Martini, and titled, “Future environmental and biological scenarios between the Mediterranean and the Red Sea.” emphasized that the Mediterranean Sea and the Red Sea present fundamental environmental and biological differences, but they also have similarities. “It is about the future of the environment of the Mediterranean on the basis of what is happening in the Red Sea, it highlights the similarities between the seas and the environmental changes and issues they face as a result of climate change”, said Consul Martini. The opening of the Suez Canal and the rise of the Mediterranean temperature are bringing tropical species typical of the Red Sea into the Mediterranean Sea. Hence the Red Sea is considered a research subject to comprehend future environmental and biological scenarios in the Mediterranean, in the light of climate change.

Left to right: Dr. Folco Giomi, KAUST ARTmosphere curator Solkem N’Gangbet, Prof. Daniele Daffonchio and Prof. Giorgio Bavestrello

Professor Daffonchio presented insights into deep sea anoxic brine lakes, considered to be among the most extreme aquatic environments on Earth. “The organismal diversity and metabolic potential of the microbial assemblages in the brine pools are exciting models to disentangle the symbiotic and syntrophic cooperation between microorganisms to sustain element cycles in the deep-sea desert. The brine lakes offer exciting models for the understanding of the ecological relationships among microbes in extreme environments.” said Prof. Daffonchio. The conference also featured presentations by Giorgio Bavestrello, Professor of Zoology at the University of Genoa, discussing global warming and structural changes in benthic communities in the Mediterranean and Dr Folco Giomi, Researcher in Ecology at the University of Padua discussing anthropogenic driven climate warming as a global threat for ocean systems. The conference was sponsored by the Italian Consulate General in the framework of the initiative “Italy, Culture and the Mediterranean” and the KAUST Red Sea Research Centre, with the aim of connecting Italian scientific community in KAUST and Italian universities, in addition to communicating research findings to new audiences.

12 | Recent Events

Roberto Arrigoni awarded “Benazzi Lentati” in Zoology by Academia dei Lincei Dr. Roberto Arrigoni, a research scientist in the Red Sea Research Center (RSRC), has been awarded the international prize “Benazzi Lentati” in Zoology, by Accademia dei Lincei (Rome, Italy) in June 2018. Accademia dei Lincei is the oldest scientific association in the world, founded in 1603 by Federico Cesi. His great desire was to explore the secrets of nature with a perception as acute as that of the lynx. Hence the arms and the name “Lincei” attached to their association. The biennial international prize “Benazzi Lentati” is dedicated to international young researchers (below 35 years old) in the field of organismic evolutionary zoology. The price is named after Giuseppina Benazzi Lentati and Mario Benazzi, two important Italian zoologists working on platyhelminthes, and former members of Accademia dei Lincei. Dr. Arrigoni was awarded the prize with the following motivation: “The candidate has studied the subject of the ongoing threats to the coral reef ecosystem in several biogeographic area of the Indo-Pacific, considering different aspects such as ecology, systematics, evolution, and genetic diversity. In particular, he focused his attention to scleractinian corals, the most important reef builders worldwide. In this well-structured approach, he used both molecular and morphological methods that led him to discover and describe new species and their phylogenetic relationships.”

Dr. Roberto Arrigoni Research Scientist Reef Ecology Lab

13 | Awards

Roberto received the prize during the closing ceremony of the academic year of Accademia dei Lincei, which took place in Palazzo Corsini. Sergio Mattarella, President of the Italian Republic, and Sergio Costa, Minister of Environment, were present. The ceremony was followed by a refreshment at Villa Farnesina, a Renaissance suburban villa hosting famous Raphael’s frescoes, including The Triumph of Galatea and Cupid and Psyche. Roberto Arrigoni joined KAUST in March 2015 as post-doctoral fellow in Reef Ecology Lab of Professor Michael L. Berumen and he is currently a research scientist in the same group. His main studies address systematics, phylogeny, and biogeography of scleractinian corals from the Indo-Pacific, with a particular focus on the Red Sea coral fauna. He is interested in the integration of genetics and morphology to evaluate coral biodiversity and to enhance the field of coral taxon.

Left to right: Prof. Maurizio Brunori, vice-President of Academia dei Lincei, Prof. Alberto Quadrio Curzio, President of Academia dei Lincei and Dr. Roberto Arrigoni

Annual ceremony of the Lincean Academy, Rome, Italy.

The award recieved by Academia dei Lincei

14 | Awards

Upcoming Events • New students academic orientation (August 12 - 14) • First day of classes (August 26) • FEP: Marine biodiversity (October 21 - 23) • Workshop: The future of Red Sea biodiversity (October 23 - 25) • RSRC Open Science Conference (November 26 - 27) • Conference: Securing a future for Red Sea ecosystem (March 11 - 13)

Contact Us rsrc.info@kaust.edu.sa seda.gasparyan@kaust.edu.sa www.rsrc.kaust.edu.sa Red Sea Research Center (RSRC) King Abdullah University of Science and Technology (KAUST) Ibn Al-Haytham (building 2) Thuwal 23955-6900 Kingdom of Saudi Arabia

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