The Role of Coral Reefs, Photosynthesis, and Predators on the Origin of Parasitism

The diversity of the microbial world is significantly greater than the combined diversity of all macroscopic plants, animals, and fungi, but we know next to nothing about most of it. As a result, purely hypothesis-driven research can be limited by the fact that we do not even know many of the right questions to be asking. Even our understanding of the best-studied microbes, typically human pathogens, can be turned on its head with a single discovery. Here, I will discuss one example relating to the evolutionary history of the apicomplexans, the lineage including the malaria parasite, Plasmodium. Plasmodium and its relatives can only survive by infecting and living inside animal cells. Given this lifestyle, as well as over 100 years of intensive study, it came as a surprise when Plasmodium and other apicomplexans were found, by chance about a decade ago, to contain a plastid or chloroplast - the intracellular compartment where photosynthesis takes place in plants and algae. These parasites live in the dark, so why a plastid? And from where? A decade of work on these questions has revealed much about its function, but its convoluted evolutionary history, peppered with odd characters and plot twists, remained more problematic. Apicomplexans have long been known to be distant relatives of photosynthetic dinoflagellate algae and colpodellid predators who suck the cytoplasm from their prey, but recently another group was discovered that changed much about our understanding of their evolution. These are the “chromerids”, who seemingly invade corals using a similar infection mechanism as apicomplexans, but rather than killing their host, they symbiotically provide them with food. Although chromerids were unknown until recently, it turns out that their genes have previously been gathered in large-scale environmental surveys of microbial diversity. But the biology of eukaryotes is impossible to interpret from sequence alone, and without the basic biological information provided by observing cells (e.g. cultured chromerids in this case), the information held within these genes was impossible to interpret correctly. It took only two well-characterised chromerids, however, to make this information at least partially accessible, and now we can use these benchmarks to address a variety of questions about where and how these organisms live. This has in turn fed into new ideas about how the apicomplexan parasites originated in a marine environment, and how both coral symbioses and photosynthesis might have played important roles in this evolutionary transition.