Coral Microbiomes through Space and Time
Jesse Zaneveld, Oregon State University
Coral reefs face increasing challenges worldwide, with more than a third of coral species threatened by extinction. These threats are important because several billion people rely on reefs as a primary protein source, and because many marine organisms depend on reefs at some portion of their lifecycle. A variety of overlapping culprits in coral decline have been identified, including overfishing and nutrient pollution, which fuel growth of algal competitors of corals, and periods of extreme temperature. I will discuss two projects that examine how coral’s complex relationships with microorganisms affect the response of coral colonies and coral species to these environmental challenges.
Why study the microbial communities of corals? We now know that animal life evolved in the context of immense microbial diversity, and that microbial symbiosis plays diverse and important roles in animal physiology. Gut microbial communities help process the varied diets of animals ranging from leaf-cutting ants to baleen whales. Microbial action allows some animals, such as woodrats, to feed on otherwise poisonous plants, thereby affecting the range over which they can spread. Amazingly, microbial symbionts also often influence animal behavior, with examples ranging from mate choice in fruit flies to social anxiety and compulsive behavior in mice. In corals, microbiological studies have documented key roles in energy harvest and defense against pathogenic bacteria and fungi. However, much remains to be uncovered. Reef building corals have diversified for more than 220 million years – far longer than mammals and somewhat longer than flowering plants – but the overall evolutionary history of corals and their microbes is little studied. As part of the Global Coral Microbiome Project, we are currently collecting DNA samples (more than 1000 to date) from all major groups of corals across 15 locations worldwide to study how these communities evolved over evolutionary time, and to ask whether the microbial symbiosis can help us understand the relative vulnerability or resistance of coral species to environmental stress.
Coral symbiosis also has a dark side: thermal stress is well known to kill corals by disrupting symbiosis with photosynthetic Symbiodinium symbionts, and laboratory experiments have further suggested that algae may kill corals in part by disrupting their microbial communities. Thus understanding the ecology of coral-microbe symbiosis will be important for coral conservation. However, the relationship between human activities and coral microbiology have been challenging to test experimentally under field conditions. We conducted a three-year experiment in the Florida Keys applying nutrient pollution or simulated overfishing to reef plots, and tracing effects on reef communities, coral microbiomes, and coral health. The results show that extremes of temperature and algal competition both destabilize coral microbiomes, making them more vulnerable to takeover by pathogens- a pattern that closely resembles the effects of immune compromise in humans or other primates. This destabilization is most severe in coral colonies that lost tissue, and also correlated with visible signs of coral disease. Thus, overfishing and nutrient pollution disrupted reef communities all the way down to microbial scales, greatly increasing coral tissue loss, disease, and death. In a surprising twist, these local stressors interacted with temperature: the greatest microbiome disruption occurred and 80% of coral mortality happened in the hottest periods. Thus local stressors and seasonal temperature extremes, which are predicted to increase with climate change, likely interact to disrupt coral microbiomes, contributing to coral decline.
Preserving coral reefs will depend on input across diverse disciplines. It is my hope that better understanding coral’s fascinating associations with microorganisms will play a role in helping to inform conservation efforts, and deepen our appreciation for these biological wonders.