The Microbe That Invaded Caribbean Coral Reefs

Think of giant pythons from southeast Asia, ending up in the Florida everglades and suffocating any small mammal they could find. Think of cane toads from South America, relentlessly marching over Australia, swallowing bird eggs and native frogs. Think of rats from pretty much any mainland country, stowing away onto pristine islands and eating their way through the helpless local birds. These are all classic examples of invasive species.

Here is another, and it’s very different. It’s a microscopic alga called Symbiodinium trenchii. Unlike the python or the cane toad or the rat, this tiny brown bauble seems fairly benign—even beneficial. It lives in the cells of corals and provides them with food, by harnessing the sun’s energy to make sugars. It typically does this in its native waters in the Indo-Pacific Ocean. But somehow, it recently found its way to the Caribbean, on the other side of the world. And there, it displays all the characteristics of an invasive species.

Tye Pettay from Pennsylvania State University has shown that S.trenchii has spread through a large number of Caribbean corals. It provides its hosts with nutrients but is less generous than the native coral-associated algae that is has displaced. It is especially common in populations that have been ravaged by heat or pollution or disease. It looks for all the world like an opportunistic infection, of the kind that takes hold in people whose immune systems have been weakened. “It’s all over the Caribbean and it’s not going away,” says Todd LaJeunesse, who led the study.

Corals are stinging colonial animals that form partnerships with many species of Symbiodinium algae. These allies—these symbionts—provide them with the energy they need to construct their impressive reefs. But if oceans get too hot, the corals evict their symbionts, losing a source of both energy and colour. That’s why they are said to be “bleached”. If they stay too long in this condition, they die. Solitude is no life for a coral.

But there’s a way out. Some Symbiodinium species make their coral hosts more tolerant to heat and other stressful conditions. If a coral can swap its algal partner for a hardier one, it could survive.

This is what happened in 2005. That year, the Caribbean experienced exceptionally high temperatures; as a result, more than 80 percent of its corals bleached. It was a catastrophe, but for S.trenchii, it was an opportunity. In the months before the bleaching event, LaJeunesse found this species in less than 1 percent of the corals. During the event, he saw it in 20 percent of them. “We found it in the most severely stressed animals,” he says. “We have never seen it behave like this elsewhere.”

Through almost a decade of work, LaJeunesse’s team has confirmed that S.trenchii does indeed behave very differently in separate parts of the world. In the Indo-Pacific, it exists as a genetically diverse population, which has probably been around hundreds of thousands of years—if not millions. It is not alone, either. S.trenchii is part of a lineage of Symbiodinium called “Clade D”, which arose in the Indo-Pacific Ocean and diversified into many species, each of which associates with certain types of coral.

In the Caribbean, things are very different. S.trenchii is the only member of Clade D around, and it lives inside a wide variety of coral hosts. This population has absurdly little genetic diversity. Even across hundreds of kilometres of oceans, individual cells of S.trenchii are almost identical. It’s like looking at a sea of clones.

S.trenchii must have hitched a ride to the Caribbean on some kind of ship, perhaps as recently as a few decades ago. It then spread across the entire region, perhaps taking advantage of the rough times that the local corals were experiencing. “The poor Caribbean has been trashed with sea surface temperature anomalies and pollution and a huge human population,” says LaJeunesse. “It’s severely degraded. If it were pristine, if we went back 100 years, I’m not sure S.trenchii would be so successful.”

But we can’t go back, and it is successful. “It is what it is,” says LaJeunesse. “There’s nothing we can do about it.” And indeed, we might not want to do anything about it. There’s a tendency to view all invasive species as villains, but they’re not all like cane toads or Burmese pythons. There’s some evidence that these invaders can have positive effects on their new homes. Take S.trenchii. You could argue that its invasion benefited the corals, by allowing them to weather the warm spell of 2005.

This silver lining comes with a cloud. Pettay’s experiments showed that S.trenchii is a more selfish partner than the native algae of the Caribbean. It produces just as much sugar as its peers, but it hands over much less to its coral partners. As a result, the corals can only build their rocky reefs at half their usual rate. It might be better for them to have a stingier partner than no partner at all, but in the long-term, incompatibilities with S.trenchii might ultimately harm them and the reefs that they build. For now, no one knows where the balance of benefits and risks lies.

LaJeunesse wants to find out. He wants to know how S.trenchii affects the growth rates of its coral hosts. Also, what makes it such a good invader? And why is it hardier than other related species? “It’s the only member of Clade D whose genome has been duplicated,” he says. “It’s speculative, but maybe that’s something to do with it.”

He also wants other coral biologists to pay more attention to the microbial side of the coral-algal symbiosis. Many of them talk about corals “choosing” or “shuffling” their symbionts, as if the symbionts were passive halves of their own partnership. “It drives me crazy,” he says LaJeunesse. “I think people work on corals because they like corals, so they take the host’s point of view.”

But the symbionts are incredibly complex, too. They aren’t just bacteria; they are very complex organisms. They have as much DNA in their cells as you do in yours, and even more genes. Humans and corals have just over 20,000 genes in their genome; Symbiodinium has between 40,000 and 50,000, and we have no idea what around half of those do. “Who is the master of this house?” asks LaJeunesse.

Reference: Pettay, Wham, Smith, Iglesias-Prieto & LaJeunesse. 2015. Microbial invasion of the Caribbean by an Indo-Pacific coral “zooxanthella”. PNAS http://dx.doi.org/10.1073/pnas.1502283112