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Photo Credit: Robin T. Smith, Science Under Sail Institute for Exploration.
science-journal
Chimeric Coral
Classifying the remarkable partnerships that could render resilience to warming waters
6 May 2019

Great monuments and structures of red, orange, and brown fold and branch and spread in an almostalien scene, forming a floor of sorts as a myriad of creatures moves past in a blur in this literal ocean of color.

SMALL, GOLDEN-BROWN MICRO-ALGAE live symbiotically inside the cells of coral, providing the coral with nutrients. Although these symbionts all look very similar under a microscope, they are part of a group that contains hundreds and possibly thousands of species. Photo Credit: Todd LaJeunesse

SMALL, GOLDEN-BROWN MICRO-ALGAE live symbiotically inside the cells of coral, providing the coral with nutrients. Although these symbionts all look very similar under a microscope, they are part of a group that contains hundreds and possibly thousands of species. Photo Credit: Todd LaJeunesse

“It was overwhelming. There were so many different colors and kinds of animals, I wasn’t sure where to look.”

Coral researcher Todd LaJeunesse vividly recalls his first trip to the Great Barrier Reef off the coast of Queensland, Australia, in the early 2000s. He had spent years studying reefs in the Caribbean but wasn’t prepared for the stunning diversity of species found among the reefs near Heron Island. The expansive waters of the Pacific Ocean along with the geologic history of the area allow the Great Barrier Reef to support more than 400 species of corals and 1,500 species of fish—many times the number of species found at Caribbean reefs.

“The diversity at the Great Barrier Reef is incredible,” said LaJeunesse. “But I remember going back to Heron Island seven or eight years later and thinking that it wasn’t the same. Areas that were once vividly colored with living coral had died in response to environmental degradation. These declines in reefs have also been scientifically documented over the last 30 years, and that’s concerning. In less than a human lifespan, we’re seeing changes that would normally take place over thousands of years.”

Within the Great Barrier Reef, back-to-back environmental events in 2016 and 2017 led to anywhere from 15 percent loss of coral cover in the central parts of the region to as much as 50 percent in the northern Great Barrier Reef, according to the Australian Institute of Marine Sciences.

And reef declines are not limited to the Pacific Ocean; they have been documented across the planet. Reefs worldwide face a variety of threats, including local threats like pollution, overfishing, and those that recently impacted the Great Barrier Reef, like typhoons and invasive species. Globally, reef ecosystems face a major challenge in the form of climate change, which is raising water temperatures worldwide. Warming ocean waters threaten the remarkable partnership that forms the basis of reef ecosystems, a partnership that has developed over millions and millions of years.

“Corals form the foundation upon which everything in the reef ecosystem is built,” said LaJeunesse. “But what we think of as corals are really a chimera of two very different organisms: the coral itself and the microscopic algae that live within their cells. The coral cannot live for long without their intracellular residents, which provide up to 90 percent of the coral’s daily nutritional needs by photosynthesizing sunlight. Together, the corals and the microalgae form a tight mutualistic symbiosis. Warming water affects the physiology of both the coral and their microalgal symbionts and thus affects this important partnership. It would seem that their greatest strength is also their greatest weakness.”

Understanding how corals and their symbionts might respond to climate change is critical, as reefs protect coastal regions from storms and wave erosion, provide food and tourism revenue to local communities, and act as a source of many compounds used in pharmaceuticals, from cancer drugs to sunscreen and beauty products.

“When researchers started to apply genetic techniques in the 1980s and 1990s to try to better understand the coral-algae partnership, we realized that we weren’t looking at one species of symbiont as was previously assumed,” said LaJeunesse. “We now realize that there are hundreds or perhaps thousands of different symbiont species. Less than 1 percent of them have been characterized using genetics and other traditional techniques of taxonomy and systematics.”

In order to understand how climate change affects reefs, researchers need to better understand the relationship between corals and their symbionts and how they evolved together. They need to know about the physiology, ecology, and geographic distribution of the symbiont species and how they enter and interact with their coral hosts—information that improves models that forecast the response of corals to climate change. And to do all that, they first need to know what symbiont species are out there.

 

Classifying symbionts

The single-cell symbionts that reside in corals, sometimes called zooxanthellae, are members of the dinoflagellate family Symbiodiniaceae. Other kinds of dinoflagellates include planktonic species that discolor the water, causing toxic red tides when they bloom. Even though analyses of DNA in the early 1990s began to reveal the large and ancient diversity of the symbionts, few species were characterized over the following decades.

“Simply by swimming over a coral colony, I can usually identify the genus and often species of the coral by its physical characteristics, but the symbionts essentially all look the same under a light microscope,” said LaJeunesse. “With genetics, we can easily tell the difference and use these data to help describe new species. I sometimes feel as if I’m living in the 1700s or 1800s, when so many new species were being described by natural historians and contemporaries of Charles Darwin. In our research, almost everything is a new discovery when studying coral symbionts.”

LaJeunesse and his team have taken on the daunting task of starting to separate out and describe some of the most common and widespread symbiont species. Together with their global network of collaborators, they have collected DNA samples from corals and their symbionts found all over the world—from the Caribbean Sea to the eastern Pacific Ocean, the Great Barrier Reef, and the Red Sea. His team has been working to update the naming scheme and classification system for the symbionts, and they have described 7 of at least 15 evolutionarily divergent groupings known as genera, some of which may contain hundreds of ecologically distinct symbiont species.

“Good taxonomy should reveal the key attributes of a species as well as its function and relationship to other organisms in an ecosystem,” said LaJeunesse. “Accurate taxonomy is critical when making accurate scientific interpretations. There was often some speculation in our field because there was no framework to set boundaries to the scientific narrative.”

The new classification system developed by LaJeunesse and his team has already made an impact on the field, helping researchers speak the same language and delve deeper into questions about the individual symbiont species, including how they respond to warming waters.

 

Rendering resilience

Pocillopora verrucosa, a type of coral.

CORALS HAVE CLEAR TISSUES that reveal the vivid pigment of the symbionts living inside their cells. When these symbionts are lost in a bleaching event, for example due to warming water, the white skeleton of the coral becomes visible. Photo credit: Todd LaJeunesse

When the water surrounding a reef becomes exceedingly warm for weeks or months—which is happening more often due to climate change—it can cause long-term physiological stress and can lead to the decoupling of the coral and its symbionts in a process known as “bleaching.” The coral’s tissue is actually clear, so the loss of most of its symbionts—whose pigmented chlorophyll gives most reef corals their brownish color—allows one to see the coral’s white skeleton.

“Then the coral must rely mostly on its stored nutrients to survive, which usually comes at a cost to its growth,” said LaJeunesse. “The symbionts can repopulate throughout the coral when the stress is gone, but it takes time. If the coral runs out of its nutrient stores before the symbionts repopulate, it starves or becomes susceptible to terminal diseases from being severely weakened.”

Some symbionts, it turns out, offer protection against warming waters. If these heat-tolerant species could disperse and populate corals in areas where waters are beginning to warm, they could potentially provide a rapid way for corals to deal with warming. LaJeunesse and his team are working to understand where these tolerant symbionts occur and how they offer resilience to warming.

One symbiont species in particular, Durusdinium trenchii—a generalist species that can occur in many kinds of corals—has found its way into the Caribbean from its native Pacific waters and has spread throughout the region. The species appears to offer a measure of thermal tolerance to the corals it inhabits.

“This species provides thermal tolerance to some colonies of coral in waters up to several degrees Fahrenheit higher than normal, which is a lot for the coral,” said LaJeunesse. “A coral colony tends to be dominated by a single stable symbiont, but other species like D. trenchii may occur in trace amounts. What is probably happening is that, as temperatures increase, the native symbiont allocates its resources to cope with the stress of warming instead of toward cell division. The invasive symbiont is not as bothered by the stress of the temperature change and continues to divide. In a short time, it can take over and become the dominant symbiont in the coral.

Todd LaJeunesse explores a coral reef off the coast of Mexico. Understanding the geographic distribution of both corals and their symbionts will help researchers predict how coral reefs will respond to climate change. Credit: Todd LaJeunesse.
TODD LAJEUNESSE EXPLORES A CORAL REEF off the coast of Mexico. Understanding the geographic distribution of both corals and their symbionts will help researchers predict how coral reefs will respond to climate change. Credit: Todd LaJeunesse

Durusdinium trenchii, which has incredible dispersal ability, has taken advantage of the environmental decline of the Caribbean and is becoming more prevalent in the area. This might offer some advantages, as having D. trenchii might prevent a coral from bleaching in some cases. But this thermal tolerance comes with a significant cost. LaJeunesse and collaborators, including Roberto Iglesias-Prieto, then professor of marine biology at the National Autonomous University of Mexico and currently professor of biology at Penn State, discovered that coral growth is reduced by half when D. trenchii dominates a colony.

“This symbiont may be retaining more nutrients for its own growth and physiology, which is probably why it does better in warmer temperatures,” said LaJeunesse. “But that means it’s not passing on as many nutrients to the host, compared to the native species.”

LaJeunesse wanted to know if this tradeoff between thermal tolerance and growth was also apparent in the symbiont’s native range, where the species has co-evolved with local corals. This question took his research team to the island nation of Palau in the western Pacific Ocean, where they have been studying reefs for six years.

“So far our work in Palau has yet to reveal a growth tradeoff in colonies harboring D. trenchii,” said LaJeunesse. This heat-tolerant symbiont occurs commonly in colonies growing near the shore, but it is not as common among corals in the cooler offshore reefs. However, when corals with D. trenchii are placed on barrier reefs, they appear to thrive.

“The coral grew very well offshore with the symbiont, but the relationship wasn’t stable,” said Kira Turnham, a graduate student in LaJeunesse’s lab who is involved with the experiment. “It turns out that the offshore species of symbiont ends up taking over in these corals, which suggests that competition among symbionts is playing a role. Much more than just temperature is dictating which symbiont dominates a coral.”

The team is currently investigating how factors like water quality, acidity, and the presence of trace metals required for growth affect symbionts and the competition among them—factors that could limit the potential spread of D. trenchii across the world.

Durusdinium trenchii is one of many species of heat-tolerant symbionts,” said LaJeunesse, “however, we currently don’t know what makes them so tough. This is also true of corals. Only for a handful of corals do we have extremely detailed knowledge on their basic biology, but we have very little for most others. This makes it very difficult to forecast how whole reef ecosystems will respond to climate change and warming waters.”

Some countries are taking measures to protect their coral reefs. Palau, which relies on the reef ecosystem for food, tourism revenue, and local culture, established the first shark sanctuary in the world and has closed its waters to commercial fishing. Its International Coral Reef Center also encourages researchers from around the world, like LaJeunesse, to continue to ask the important questions about corals and their place in our changing world.

“There are corals living in very warm environments in the world, which may become increasingly important in the near future, and understanding if they can proliferate and survive in areas that are being decimated by climate change comes back to basic biology,” said LaJeunesse. “There is still plenty of work to be done to understand how best we can help the builders of these important reef ecosystems.”

Lobophytum, a type of coral.