Gregory Gavelis and Gillian Gile are the 2018 prize winners of our annual competition for the best MiniReview published inFEMS Microbiology Letters. They won this year’s award with their recently published article: How did cyanobacteria first embark on the path to becoming plastids?: lessons from protist symbioses

In this interview, the Gillian and Greg detail the inspiration that led them to produce this MiniReview, the questions they hope to tackle in future reserach, and discuss the current state of this area of evolutionary biology:

Could you provide a brief, simple overview of the topic your MiniReview covers?

Photosynthesis by plants and algae is hugely important on Earth today, but photosynthesis did not originate in eukaryotes–in a sense it was “stolen.” This happened when a eukaryotic microbe (or protist) engulfed a cyanobacterium and somehow managed to pass it on to its offspring.

There is now plenty of genomic evidence that this endosymbiosis took place (more than once in fact!), but the timing, ecological context, and pretty much every other detail is up for debate. A lot has been written about the intricate machinery that exchanges proteins and metabolites between chloroplasts and the rest of the cell – especially in modern plants. But that raises these questions:

• How did their protist ancestor maintain an endosymbiont before this machinery evolved?
• How did it exchange nutrients (without the cyanobacterium being digested) and which metabolites were important?

We are fortunate to live in a world where modern protists host a range of symbiotic interactions, many of which might not be familiar to folks working on model organisms. So we surveyed some of those symbiotic examples (and interesting experiments) to try to shed light on the early junctures of eukaryotic photosynthesis.”

 

Why is it important for us to learn about the history of these microbiological processes?

We live in a solar-powered biosphere, where even non-“green” fuel sources like petroleum and natural gas are the legacy of ancient algae.

Algae are still far more efficient at capturing solar energy than our newest technologies, but their ancestors were not always so adept – especially during the earliest stages of endosymbiosis (though starving or being damaged by an endosymbiont’s oxyradicals would have provided a big incentive to improve).

As evolutionary biologists, we are interested in algal origins purely out of curiosity, but this area of study may also uncover lessons that humankind can use as we transition to greener technologies, some of which make use of algae and bacteria, sometimes in co-culture with other microbes.

 

What encouraged you to review research within this area of microbiology?

Actually, it was a single study by Christina Agapakis (et al. 2011) in which she engineered a cyanobacterium to be taken up by animal cells, as a kind of “synthetic chloroplast.”

The promise of that approach to evolutionary biology is pretty thrilling, i.e. by putting a cyanobacterium in a protist we could “reenact” the origin of eukaryotic photosynthesis.

This has proven much easier said than done, but in the process of preparing, we realized that her study was the latest in a very interesting vein of experimental work on endosymbiosis.

This work, which we reviewed here, has been somewhat overlooked in our evolutionary subfield. Its spirit of wild experimentalism is very appealing to us, as researchers who usually view endosymbiosis retrospectively (i.e. by looking at the genomic footprints of ancient endosymbiotic events).”

 

What do you see as the next steps in this area of research?

To finish what she started. To make a protist-cyanobacterial system where the endosymbiont is heritable, as an early-chloroplast model.

Honestly, we really bit off more than we could chew with that idea. But we have been fortunate to work with very talented cyanobacterial researchers who have enthusiastically taken up the cause.

Engineering a cyanobacterium is absolutely the biggest challenge, since they are not nearly as user-friendly as say, E. coli. In fact, since our review came out, a team led by Mehta (et al. 2018) successfully established E. coli in a respiration-deficient mutant of yeast, as a sort of model of early mitochondria (which evolved from alpha proteobacteria).

So engineered symbioses are finally happening!”

 

What is the most important unanswered question in current research into the science and history of photosymbiosis?

It’s not a matter of any one question, as much as how we are answering the questions.

There is no shortage of genomically-informed hypotheses about which transporters and which metabolites first interwove the metabolism of a cyanobacterium and a protist.

Ultimately though, none of these hypotheses have been tested experimentally, because we have no cyanobacterial-protist system that is at the right juncture of endosymbiotic integration.

Genomic surveys have given us no end of fodder for evolutionary speculation, but until we find a way to test hypotheses experimentally, these explanations are fragile and insubstantial, like castles in the sky.”

Citation: Mehta, Angad P., et al. “Engineering yeast endosymbionts as a step toward the evolution of mitochondria.” Proceedings of the National Academy of Sciences 115.46 (2018): 11796-11801.

Read the 2018 award winning MiniReview: How did cyanobacteria first embark on the path to becoming plastids?: lessons from protist symbioses