- Open Access
Genome of tiny predator with big appetite
© The Author(s). 2018
- Published: 28 November 2018
The original article was published in BMC Biology 2018 16:137
The capture and enslavement of eukaryotic algae by unicellular predators to acquire photosynthesis was a major driving force in early eukaryotic diversification. A genome presented in BMC Biology provides a glimpse of how such a tiny predator might have preyed on red algae and detained them to create new lineages of photosynthetic organisms.
To get DNA sequences from organisms one typically needs a goodly amount of them. Goniomonas is a predator, so when Hill and I wanted to grow it up in large numbers, we opted to provide it with loads of bacteria to engulf and digest—this was as simple as me popping a grain of wheat into several flasks of culture media to support bacterial growth, whilst Hill arduously plucked out individual Goniomonas cells with a micropipette and placed them in solitary confinement with only food for company. Hill and I got a clonal culture and a ribosomal RNA sequence from Goniomonas truncata, and could show it was sister to photosynthetic cryptomonads .
In their recent article in BMC Biology, Cenci et al. report the entire genome of a related species, Goniomonas avonlea , which hails from the setting of Lucy Montgomery’s novel Anne of Green Gables. The G. avonlea genome paints the first complete picture of how cryptomonads might have functioned before they crossed the tracks and made a pact with an alga to become autotrophic. It is a fascinating window into how things probably were with cryptomonads before they switched lifestyles.
As genomes go, the G. avonlea blueprint is still a bit of a roughie, remaining in ~ 32,000 unjoined pieces. That’s because the genome is huge for such a tiny organism, with a final size approaching 100 megabases; the effort to get it fully assembled and polished would be formidable. Gene count, at ~ 18,000 non-redundant proteins, is also impressive, and these genes are, on average, interrupted by about five introns each. But numbers aside, what does the genome tell us about how G. avonlea makes its living, now and in the past? Quite a bit as it happens. A concerted search turned up no convincing evidence for G. avonlea now having, or ever having had, a plastid. Thus, we can be pretty certain this type of cryptomonad is ancestrally heterotrophic. Metabolic pathways typically taken care of by the plastid in plants and algae—namely fatty acid synthesis, isoprenoid precursor synthesis, iron sulfur cluster generation, and heme synthesis—are apparently done in the cytosol of G. avonlea using canonical eukaryotic machinery not related to cyanobacteria. Thus, there are no traces of plastid-type metabolisms lurking in the genome, and Goniomonas appears to be a living representative of the pre-secondary-endosymbiosis cryptomonads.
G. avonlea also seems well equipped gene-wise to digest its prey, having a panoply of lysozymes to chew through the cell walls of those bacteria unfortunate enough to end up going down the gullet of the predator and into its food vacuoles. For me though, the jewel-in-the-crown of the G. avonlea genome are glycan hydrolases belonging to the GH50 family, which cleave β-1,4 glycosidic bonds of agarose, a principal component of red algal cell walls. G. avonlea thus seems equipped to be algivorous, capable of digesting the walls of red algal prey cells. In today’s oceans and streams, most red algae are multicellular and too large to be preyed upon by a miniscule flagellate like G. avonlea, but unicellular red algae small enough for a Goniomonas cell to engulf are not uncommon and were perhaps more so in earlier times. Thus, if G. avonlea does indeed engulf and digest red algae, it is not too much of a stretch to imagine a scenario where the prey cell is detained and not digested—exactly the kind of event predicted to have occurred at the outset of a secondary endosymbiosis creating the photosynthetic cryptomonads [2, 3].
Goniomonas is thus a nice fit for the ancestral phagotroph that was routinely capturing and digesting red algae and could have commenced a longer and more sustained relationship with its prey to embark on the acquisition of photosynthesis through a secondary endosymbiosis. But what does Goniomonas tell us about the other, non-cryptomonad eukaryotes that also have reduced red algal endosymbionts for plastids?
Major eukaryote groups including the heterokonts/stramenopiles (algae like brown kelps, diatoms, and golden flagellates), haptophytes (abundant limestone-armoured phytoplankton whose dead ancestors comprise most of the white cliffs of Dover), dinoflagellates (including the symbionts of corals crucial for reef building and the toxic basis of certain red tides), and alveolates (parasites of animals and protists that cause diseases such as malaria and toxoplasmosis and possess relic, non-photosynthetic plastids) all harbour secondary endosymbionts of red algal origin. A long-standing debate about whether all these different types of organisms gained their red algal endosymbiont in one event—perhaps akin to the one discussed here in which a Goniomonas-like phagotroph captured and retained a red alga—or whether each of them descends from a separate capture of a red alga by different ancestors remains wide open, despite 40 years of investigation [8–10].
The genome of Goniomonas doesn’t yet resolve this debate, but it gives us an extant model with which to explore what the phagotrophic partner in the extraordinary amalgam that led to at least one group of complex algae, the cryptomonads, was like. We might just have extant descendants of the two partners—predator and prey—with which to better understand how a great swathe of eukaryotic diversity originated through secondary endosymbiosis. Maybe we should feed our Goniomonas on red algae rather than bacteria.
GIM is supported by an Australian Research Council Laureate Fellowship.
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GIM wrote the manuscript. GIM read and approved the final manuscript.
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