Exploring dinoflagellate biology with the awesome power of yeast genetics
Dinoflagellates are the only group of eukaryotes to have abandoned histones as their primary DNA packaging proteins. This represents a major enigma in evolutionary biology as histones are some of the most highly conserved proteins known. By using yeast as a model organism, we found that histone loss in dinoflagellates could have been an adaptive response to viral infection. Our results emphasize the usefulness of model organisms in studying the biology and evolution of diverse and hard-to-work-with eukaryotes.
Ask anyone who has experimented on dinoflagellates how their experience went and you will likely receive a disgruntled sigh, shudder, or perhaps even a single tear. But why is this so?
The dinoflagellates represent a phylum of remarkable single-celled algae found in aquatic environments where they contribute heavily to global photosynthesis, participate in essential symbioses with corals, and form harmful algal blooms. However, it is their unique cell biology that makes them truly mysterious and this has attracted cell and molecular biologists for decades. For example, these organisms are often encased in an elaborate cellulosic armour which can house complex subcellular structures such as eyes (Gavelis et al. 2015), harpoon guns (Gavelis et al. 2017), and some of the most unconventional nuclei ever observed.
Figure 1. The armoured dinoflagellate, Ceratocorys horrida (left panel) and an electron micrograph of a dinoflagellate chromosome (right panel, image courtesy of Greg Gavelis).
Unlike all other eukaryotes, dinoflagellates have abandoned the use of histones as their major genome packaging proteins and instead have replaced them with viral-derived proteins termed DVNPs (Dinoflagellate-Viral-Nucleoproteins). This transition appears to have led to dramatic changes in chromosome structure as dinoflagellate chromosomes are permanently condensed and exist in a liquid crystal phase capable of polarizing light. But despite the magnitude of this transition, how and why these changes occurred has remained unclear, largely due to the technical challenges associated with studying dinoflagellates.
Working with dinoflagellates often leaves the impression that they are out to get you. These little saboteurs have evaded the development of genetic transformation methods, and their genomes are so large and complex that assembling even the smallest dinoflagellate genome has posed significant challenges. Even procedures such as PCR and routine culturing are frequently foiled as a result of their genome characteristics and complex ecology.
To get around these issues and to try to gain insights into dinoflagellate chromatin evolution, we employed one of the most classic tools in biology, the model organism Saccharomyces cerevisiae. We examined how the transition between histone- and DVNP-based chromatin could have occurred by expressing DVNP in yeast and characterizing how it interacted with canonical chromatin. Using a combination of high-throughput sequencing and genetic screens we found that DVNP causes histone loss by binding the yeast genome and displacing histones. This impairs the growth of yeast, but this toxicity can be reduced by decreasing the amount of histones in the cell. These data suggest that dinoflagellates could have depleted their histones as an adaptive response to exposure to DVNP, perhaps following viral infection.
Although we were spared from working directly with the dinoflagellates, these results did not come easily. Like the dinoflagellates, model organisms carry their own challenges such as the abundance of data they generate and the care required to avoid artifacts and ensure reproducibility. Therefore, model organisms are evidently a useful and underutilized tool for studying diverse eukaryotes such as dinoflagellates, but direct experiments in the organisms of interest will always be required to complement model based approaches. I believe a combination of these methods will help us dissect the complex biology of these organisms and allow us to better understand the molecular diversity and evolution of eukaryotic life.
You can view our open access article in Nature Communications, at: http://doi.org/10.1038/s41467-018-03993-4
The poster image was adapted from Haeckel (1904).
Gavelis et al. Eye-like ocelloids are built from different endosymbiotically acquired components. Nature, 523, 204-207 (2015).
Gavelis et al. Microbial arms race: Ballistic “nematocysts” in dinoflagellates represent a new extreme in organelle complexity. Science Advances, 3, e1602552 (2017).