Sleep is essential for much of the animal kingdom. During the night, neuron and tissue repair mechanisms are activated to aid recovery from daily activity. This is risky: organisms that sleep are more vulnerable to predators. However, the phenomenon extends from mammals to invertebrates. Nevertheless, until now it was not known whether other, more ancient groups without neurons, such as corals, engage in any kind of nocturnal rest.
A study led by the Institute of Evolutionary Biology (IBE) , a joint research center of the Spanish National Research Council (CSIC) and Pompeu Fabra University (UPF) , has revealed that corals also sleep, despite them not having a nervous system, while their microbiome remains awake.
For the first time, a biological day-night pattern that transcends the individual and helps sustain a symbiotic relationship has been identified in situ. Corals need to rest between sunset and sunrise to recover from the oxidative stress caused by their microbes during daylight hours, when they nourish them through photosynthesis.
The research, carried out by the group of Javier del Campo, principal investigator at the IBE (CSIC-UPF), suggests that sleep is an older evolutionary mechanism than previously thought, and it could have been contributing to maintaining the balance of host-microbe relationships billions of years ago.
Day and night in coral symbiosis
The work was carried out on the living coral reef off the island of Curaçao (Caribbean Sea), where the brain coral Pseudodiploria strigosa and its symbiont, the alga Breviolum - which lives inside its cells and provides it with nutrients when it photosynthesizes -, were studied.
To carry out the research, the team made dives every six hours over a three-day period, to a depth of about five meters and, for the first time, studied the activity of the coral and its microbiome in situ during the day and night.
Every six hours they analyzed the gene expression of the coral and its symbionts and discovered that the host sleeps at night, despite having no nervous system. "P. strigosa sleeps for a third of the day, like humans, and the day-night cycle regulates its biological clock, known as the circadian rhythm", explains Bradley Allen Weiler, first author of the study and previously a predoctoral researcher in del Campo's group at the IBE (CSIC-UPF). But while the coral rests, its microbes remain active and mostly stable.
Corals sleep to stay in balance with their microbes
When darkness falls, corals activate mechanisms to repair DNA damaged over the course of the day. In daylight, the symbionts photosynthesize within the coral cells. As a result, they produce organic matter that nourishes the coral, but they also generate reactive oxygen species that can damage both tissues and the host's genetic material.
By sleeping, the corals minimize these effects and balance their relationship with the microbes. "At night, the corals repair DNA damaged by their symbionts," says del Campo, also an associate professor at the Rosenstiel School of Marine and Atmospheric Science at the University of Miami. "The microbes stop photosynthesizing, but they maintain other cellular functions and do not need a long rest."
The study shows how mutualistic relationships can be beneficial, despite having side effects. Coral sleep allows it to recover from daily damage, and sustains a symbiosis over time that, without this rhythm, would be toxic. "It is possible that these microorganisms became trapped inside coral cells billions of years ago, and that this contact ended up giving rise to a mutually beneficial relationship. However, these relationships are not intentional and if they are maintained it is thanks to certain commitments", adds del Campo.
Rethinking symbiosis: the evolutionary legacy of corals
The new research could guide restoration policies involving cultivating corals ex situ for reintroduction. "We now have a better understanding of the physiology of corals, the great architects of marine ecosystems", says Weiler. It could also help determine how microorganisms influence the animals' response to climate change.
The study confirms that sleep is an ancestral mechanism, present since the first animals billions of years ago, and that it serves to repair DNA and tissues damaged during daily activity. "We often think that only animals with a brain need to sleep, but all living beings need to repair themselves in some way. Establishing an internal rhythm that facilitates this is a very ancient and successful evolutionary strategy", adds del Campo.
For the first time, it has been shown that sleep could also be the key to maintaining relationships between species that evolved together. "This study invites us to rethink symbiotic relationships in nature and value the essential role they have played throughout evolutionary history", concludes del Campo.
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