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Green algae could hold clues for engineering faster-growing crops

Study provides insights into how algae siphon carbon dioxide from the air

Princeton University

Two new studies of green algae -- the scourge of swimming pool owners and freshwater ponds -- have revealed new insights into how these organisms siphon carbon dioxide from the air for use in photosynthesis, a key factor in their ability to grow so quickly. Understanding this process may someday help researchers improve the growth rate of crops such as wheat and rice.

In the studies published this week in the journal Cell, the Princeton-led team reported the first detailed inventory of the cellular machinery -- located in an organelle known as the pyrenoid -- that algae use to collect and concentrate carbon dioxide. The researchers also found that the pyrenoid, long thought to be a solid structure, actually behaves like a liquid droplet that can dissolve into the surrounding cellular medium when the algal cells divide.

"Understanding how algae can concentrate carbon dioxide is a key step toward the goal of improving photosynthesis in other plants," said Martin Jonikas, an assistant professor of molecular biology at Princeton and leader of the studies, which included collaborators at the Max Planck Institute of Biochemistry in Germany and the Carnegie Institution for Science on the Stanford University campus. "If we could engineer other crops to concentrate carbon, we could address the growing world demand for food," Jonikas said.

Aquatic algae and a handful of other plants have developed carbon-concentrating mechanisms that boost the rate of photosynthesis, the process by which plants turn carbon dioxide and sunlight into sugars for growth. All plants use an enzyme called Rubisco to "fix" carbon dioxide into sugar that can be used or stored by the plant.



The search revealed 89 new pyrenoid proteins, including ones that the researchers think usher carbon into the pyrenoid and others that are required for formation of the pyrenoid. They also identified three previously unknown layers of the pyrenoid that surround the organelle like the layers of an onion. "The information represents the best assessment yet of how this essential carbon-concentrating machinery is organized and suggests new avenues for exploring how it works," said Luke Mackinder, the study's first author and a former postdoctoral researcher at the Carnegie Institution who now leads a team of researchers at the University of York, U.K.




The technique enabled Engel to visualize the pyrenoid in three-dimensions and at nanometer-resolution. By comparing these images with those of liquid systems, the researchers confirmed that the pyrenoid was organized like a liquid. "This is one of the rare examples where classical genetics, cell biology and high-resolution imaging approaches were all brought together in one investigation," Engel said.



"We think the pyrenoid dissolution before cell division and condensation after division may be a redundant mechanism to ensure that both daughter cells get pyrenoids," Jonikas said. "That way, both daughter cells will have this key organelle that's critical for assimilating carbon."

To further explore how this might happen, Jonikas collaborated with Ned Wingreen, Princeton's Howard A. Prior Professor in the Life Sciences and of Molecular Biology. Wingreen and his team created a computer simulation of the interactions between Rubisco and another protein called EPYC1 -- discovered to be crucial to the pyrenoid by Mackinder and others on Jonikas' team -- which acts like glue to stick together multiple Rubiscos.


The change in the system's phase depending on the ratio of EPYC1 to Rubisco binding sites can be considered a "magic number" effect, a term typically used in physics to describe conditions where a specific number of particles form an unusually stable state. "These magic numbers, besides being relevant for pyrenoid systems, may have some currency in the field of polymer physics and potentially in synthetic biology," Wingreen said.

Wingreen and Jonikas are continuing their collaboration and hope to develop the project both theoretically -- by exploring different flexibilities and configurations of Rubisco and EPYC1 -- and experimentally, by combining the two proteins in a test tube and manipulating the number of binding sites.

"The previous thinking was that the more binding sites they have, the more the proteins tend to cluster," Jonikas said. "The discovery that there is a magic number effect is important not only for pyrenoids, but perhaps for many other liquid-like organelles found throughout nature."



The first study, "A spatial interactome reveals the protein organization of the algal CO2-concentrating mechanism," by Luke C.M. Mackinder, Chris Chen, Ryan D. Leib, Weronika Patena, Sean R. Blum, Matthew Rodman, Silvia Ramundo, Christopher M. Adams and Martin C. Jonikas, was published in the journal Cell. DOI: 10.1016/j.cell.2017.08.044


The second study, "The eukaryotic CO2-concentrating organelle is liquid-like and exhibits dynamic reorganization," by Elizabeth S. Freeman Rosenzweig, Bin Xu, Luis Kuhn Cuellar, Antonio Martinez-Sanchez, Miroslava Schaffer, Mike Strauss, Heather N. Cartwright, Pierre Ronceray, Jürgen M. Plitzko, Friedrich Förster, Ned S. Wingreen, Benjamin D. Engel, Luke C. M. Mackinder and Martin C. Jonikas, was published in the journal Cell. DOI: 10.1016/j.cell.2017.08.008

