A Widespread Coral-Infecting Apicomplexan with Chlorophyll Biosynthesis Genes
This week we profile a recent publication in Nature from Dr. Waldan Kwong in the laboratory of Dr. Patrick Keeling at UBC.
Can you provide a brief overview of your lab’s current research focus?
The lab generally focuses on major evolutionary transitions and how symbiosis, defined as two organisms living in close association with one another, has impacted them. We mostly study protists, which are microbes, but complex ones with their genome contained in a nucleus like our own (as opposed to bacteria, which have much simpler cells). Protists are very diverse and important in ecology and evolution, but relatively few people study them because they can be a lot harder to work with than other microbes. We are interested in how symbiotic relationships between protists and bacteria may have originated, how it affected the evolution of the two partners, what it did to their genomes, and what new functions might have arisen from the partnership. For example, a lot of the biochemistry in our cells for turning sugars into energy comes from a symbiotic bacteria taken up and integrated into our cells as “mitochondria” billions of years ago.
Another example is the origin and early evolution of apicomplexan parasites. Apicomplexans are an important group of obligate intracellular parasites that include the causative agents of human diseases like malaria and toxoplasmosis. They are also fascinating for an evolutionary biologist because, despite only being able to grow and divide by infecting and getting right inside the cells of their animal host, they turn out to have evolved from a photosynthetic alga, and still have a tiny relict plastid (or chloroplast), which is the compartment where photosynthesis happens in plants and algae. The plastid itself also arose by symbiosis long ago, so we have two interesting symbiosis questions in the same cell – how did they become parasites? And what happens to the plastid when its main function in photosynthesis is lost? And it gets even better because our work has led us more and more to a connection between this alga-to-parasite transition and symbiosis between algae and coral. Coral has long been known to depend on symbiosis with another alga (Symbiodinium), and the coral bleaching we hear about in the news is due to the breakdown of this relationship due to environmental stress. But many of the key players in the story of the origin of apicomplexan parasites also turn up only on coral reefs, so now we also want to know what’s the ancient symbiotic or ecological association between these parasites, their algal relatives, and coral.
What is the significance of the findings in this publication?
First, we show that the majority of corals worldwide (>70%) harbor an intracellular microbe, which we call “corallicolids”. They are tiny – invisible to the naked eye – and hide inside the cells of the coral digestive system, so have hardly been noticed before. But using environmental surveys, we found that corallicolids are the second most abundant microbial symbiont in coral tissue, after Symbiodinium (the famous photosynthetic symbiont), and thus is a key member of the long sought-after coral microbiome. This largely overlooked microbe represents an unexplored component of coral biology, and its study will reveal further insights into coral symbiosis and, ultimately, the contribution of coral-microbe interactions to overall reef ecology.
Second, we find that corallicolids may be an intermediate in the evolutionary transition from free-living to parasitic lifestyles. They are apicomplexans, but it’s not yet clear if they cause disease in corals; in fact, when we began to hunt for them it was unclear if we were looking for parasites or photosynthetic algae. We sequenced the plastid genome of corallicolids and confirmed they are not photosynthetic, but surprisingly also found that they retain the genes for making the key pigment in photosynthesis, chlorophyll. This is strongly suggestive of an intermediate state with novel biochemistry involving chlorophyll but no other components of photosynthesis, which has not been found before. Apicomplexan evolution has provided lots of surprises in the past, and this work shows it is even more convoluted than previously thought, and involves the repurposing of photosynthetic machinery for different reasons in different lineages.
What are the next steps for this research?
We do not yet know what role these organisms play in coral health, and this would be very important to find out given the conservation concerns with coral reef habitats. But we now know they are an omnipresent part of coral physiology (ie, they are found inside the tissues of most corals), so we need to know what they do. An analogy would be like discovering that a new bacteria is infecting 70% of humans in the world. One would immediately want to know what it is doing and how it is affecting us!
More fundamentally, we also want to know more about the function of chlorophyll in the absence of photosynthesis. If they are parasites (which looks likely), why make chlorophyll, and what do they do with it? This is one big mystery coming out of our paper that has interesting implications for the broader understanding of the evolution and function of chlorophyll in general, and a logical next step to study. Sequencing the corallicolid genome and working out its strange biochemistry in more detail will help both these goals and we are already working on how to do that, which is challenging since we can’t grow the organism in the lab.
This work was funded by:
This work was supported by grants and fellowships from CIHR, NSERC, the Killam Trust, and the Tula Foundation.
Images courtesy of the Keeling lab.