Innate immunity in coral symbiosis

Dr Virginia M Weis is a Professor and the Head of the Department of Integrative Biology at Oregon State University, with an extensive background in researching dinoflagellate symbiosis with marine animals such as corals and sea anemones. Her latest research focuses on extending this understanding, identifying the processes behind coral’s reaction to environmental change and stress.

Coral reefs are some of the most impressive and important ecosystems on our planet. They provide a habitat for over 25% of marine life, but they also provide a range of important services for our population, which include supporting fisheries and protecting coasts from erosion. Corals are cnidarians, a group of animals that also includes sea anemones.

Image of Aiptasia taken under fluorescent light. This animal is not stained: the fluorescence is natural. The red fluorescence is due to chlorophyll autofluorescence of the millions of dinoflagellate symbionts in the animal. The green fluorescence is a natural animal pigment.

Coral cover has seen a rapid, global decline over the past 40 years, a result of numerous stressors which can result in coral bleaching — a process in which the coral loses its symbiotic dinoflagellates (a group of microscopic and photosynthetic organisms that live within the coral’s cells and provide nutrients to their hosts). For years, research in this area has focused on the environmental stresses on corals, including climate change and ocean acidification. However, Dr Weis’ research focuses on the molecular interactions between these dinoflagellates and their coral hosts — a relationship that is at the core of a coral reef’s ecosystem.

Mutualistic relationships
Symbiosis refers to a relationship between different species that live together in a close, long-term association. For example, one species may live directly on, or in, the other. In terms of corals and dinoflagellates, the relationship is mutualistic, where both species benefit from the dinoflagellates living inside the coral. The dinoflagellates photosynthesise and provide the coral with organic carbon, whilst the coral provides a stable refuge from grazing, and inorganic nutrients and a high light environment. The inner mechanisms of coral–dinoflagellate symbiosis are currently not well understood, and yet this relationship forms the basis of many reef functions.

Dr Weis’ research focuses on the molecular interactions between dinoflagellates and their coral hosts — a relationship at the core of a coral reef’s ecosystem.

This makes Dr Weis’ research even more important. When the symbiosis between the coral and its dinoflagellates breaks down, the dinoflagellates leave the coral tissue, resulting in a “bleached” coral, which affects the coral’s calcification process. This, in turn, affects the coral’s ability to create a solid structure, which has widespread impact on the health of the reef itself. If bleached corals cannot re-establish a symbiosis with dinoflagellates they will die, which will, in turn, lead to reef destruction. One of the most important questions in this area, however, is whether it is the dinoflagellates that leave the coral when bleaching occurs, or if they are expelled by the coral itself.

Sea Anemones
Corals are not the only cnidarians that have mutualistic relationships with symbiotic dinoflagellates — there are also species of sea anemones that have such interactions. While these are very different to corals and provide different services to the environment, they are easier to cultivate in a laboratory environment than coral itself, and they also undergo bleaching. As such, they provide a good model for studying and understanding the mechanisms of symbiosis between dinoflagellates and cnidarians. This understanding could then potentially be applied to corals, further supporting conservation efforts.

Interactions at a molecular level
Through research by Dr Weis and her colleagues, a basic understanding now exists of the molecular processes responsible for the interaction between coral hosts and their dinoflagellate symbionts. The symbionts have been found to live within the digestive tract of the coral, inside compartments within host digestive cells.

Healthy reef on Heron Island, Great Barrier Reef, 2008. © Ove Hoegh-Guldberg

Transmission electron microscope image of a coral cell engulfing a dinoflagellate via phagocytosis. Pseudopods are evident partially surrounding the symbiont. For scale, alga is about 10 microns in diameter.

In some species of cnidarians, the dinoflagellate cells are passed on to offspring through the mother, but in most cases, the algae enter the host after it has been established within the reef. How do these two organisms find each other, though? On a molecular level, signalling takes place between the host and the symbiont — many cnidarians have receptors which recognise molecular patterns on the symbiont cells, allowing them to bind together. The symbiont cells enter host tissues through phagocytosis, a process in which an organism’s cells engulf a foreign body and absorb it into the body of the organism itself. This is considered to be a part of the coral’s innate immune system, which recognises and destroys damaging invaders, while also identifying and nurturing positive foreign cells.

Innate immunity
A set of genes called “scavenger receptors” (SR) have the ability to recognise numerous different microbes, and are a part of innate immunity in all animals — a system responsible for non-differential protection against damaging microbes. While humans also possess SR genes for the identification of invasive and dangerous microbes, cnidarians have been found to have a wider variety of such genes which may play a role in the recognition of symbiotic dinoflagellates by hosts.

In vertebrates, such as humans, the “complement system” recognises and destroys microbes. However, genes involved in this innate immune response have also been identified in anemones, and could have a role in the symbiotic relationship between cnidarians and dinoflagellates — although this is currently unclear.

Cnidarian-dinoflagellate research is an exciting and
developing field which will prove highly important in understanding the basis for reef and coral functions.

An important component of immunity is tolerance to microbes as well as resistance to them, and a substance known as “Transforming Growth Factor beta” (TGFβ) promotes this tolerance in vertebrates. These substances have, likewise, been found in the anemone Aiptasia pallida, and are used in regulating the interactions with dinoflagellates. When TGFβ that had been isolated from humans was added to these anemones, the bleaching response that would typically occur when the animal is exposed to heat was suppressed.

Dinoflagellate cells, when entering cnidarian hosts, “activate” a TGFβ pathway. This process is parallel to that employed by some single-celled parasites such as Plasmodium, which causes malaria, and ,em>Trypanosoma, which causes sleeping sickness. If these processes are understood in anemones, it could help to improve understanding around how these parasites enter the human body, allowing a method to be found capable of reducing parasitic infection.

Confocal microscopy of closeup of Aiptasia digestive epithelium. Red is symbiotic algae from chlorophyll autofluorescence, blue is DAPI and staining animal nuclei, green is a stain for actin filaments — staining animal tissue. For scale, algae are about 10 microns in diameter.

This area is at the forefront of cnidarian–dinoflagellate symbiosis research and is an exciting and developing field which will prove highly important in understanding the basis for reef and coral functions. Understanding these processes may help researchers to supress bleaching responses by coral and buffer against the effects of climatic and environmental change.

Future direction
Further understanding of the processes involved in this symbiotic relationship can aid in identifying the processes behind corals’ reactions to environmental change and stress, and the factors that determine a coral’s sensitivity to environmental change. This knowledge could then be used to identify how different species of coral are likely to respond to different stressors, including climate change and global warming. Ultimately, this will further aid conservation efforts in preserving and protecting these important species.

Coral reefs support thousands of species globally, and with swathes of reefs across the planet in a critical, bleached state, Dr Weis’ research is incredibly important for conserving such areas in years to come.