Researchers from Michigan State University and colleagues from University of California, Berkeley, University of South Bohemia and Lawrence Berkeley National Laboratory helped reveal the most detailed image yet important biological “antennae”.
Nature has evolved these structures to harness the sun’s energy through photosynthesis, but these sunlight receptors do not belong to plants. They are found in microbes known as cyanobacteria, the evolutionary descendants of the first organisms on Earth capable of taking sunlight, water and carbon dioxide and turning them into sugars and oxygen.
Published on August 31 in the journal Nature, the results immediately shed new light on microbial photosynthesis, specifically how light energy is captured and sent where it is needed to power the conversion of carbon dioxide into sugars. In the future, the knowledge could also help researchers eliminate harmful bacteria in the environment, develop artificial photosynthetic systems for renewable energy, and engage microbes in sustainable manufacturing that begins with the raw materials that are carbon dioxide and sunlight.
“There’s a lot of interest in using cyanobacteria as solar-powered factories that capture sunlight and convert it into some kind of energy that can be used to make important products,” said Cheryl Kerfeld, Hannah Distinguished Professor of structural bioengineering at the College of Natural Science. “With a blueprint like the one we provided in this study, you can start thinking about tuning and optimizing the light-gathering component of photosynthesis.”
“Once you see how something works, you have a better idea of how you can modify and manipulate it. That’s a big advantage,” said Markus Sutter, senior research associate at Kerfeld Lab, who operates at MSU and the Berkeley Lab in California.
The antennae structures of cyanobacteria, called phycobilisomes, are complex collections of pigments and proteins, which assemble into relatively massive complexes.
For decades, researchers have been working to visualize the different building blocks of phycobilisomes to try to understand how they are assembled. Phycobilisomes are fragile, requiring this piecemeal approach. Historically, researchers have not been able to obtain the high-resolution images of intact antennae needed to understand how they capture and conduct light energy.
Today, thanks to an international team of experts and advances in a technique known as cryo-electron microscopy, the structure of a cyanobacterial light-harvesting antenna is available with near-atomic resolution. The team included researchers from MSU, Berkeley Lab, University of California, Berkeley, and University of South Bohemia in the Czech Republic.
“We were fortunate to be a team of people with complementary skills, people who worked well together,” said Kerfeld, who is also a member of the MSU-DOE Plant Research Laboratory, which is supported by the US Department of Energy. “The band had the right chemistry.”
“A long journey full of beautiful surprises”
“This work is a breakthrough in the field of photosynthesis,” said Paul Sauer, postdoctoral researcher in Professor Eva Nogales’ cryogenic electron microscopy laboratory at the Berkeley Lab and UC Berkeley.
“The complete light-gathering antenna structure of a cyanobacterium was missing until now,” Sauer said. “Our discovery helps us understand how evolution found ways to turn carbon dioxide and light into oxygen and sugar in bacteria, long before plants existed on our planet.”
Along with Kerfeld, Sauer is a corresponding author of the new article. The team documented several notable findings, including the discovery of a new phycobilisome protein and the observation of two new ways the phycobilisome orients its light-capturing rods that had not previously been resolved.
“It’s 12 pages of discoveries,” said María Agustina Domínguez-Martín of the Nature report. As a postdoctoral researcher at Kerfeld Lab, Domínguez-Martín initiated the study at MSU and completed it at Berkeley Lab. She is currently at the University of Cordoba in Spain as part of the Marie Skówdoska-Curie Postdoctoral Fellowship. “It was a long journey full of beautiful surprises.”
One surprise, for example, came from how a relatively small protein can act as a surge suppressor for the massive antenna. Prior to this work, the researchers knew that the phycobilisome could contain molecules called orange carotenoid proteins, or OCPs, when the phycobilisome had absorbed too much sunlight. OCPs release excess energy as heat, protecting a cyanobacterium’s photosynthetic system from combustion.
Until now, there had been debate about how many OCPs the phycobilisome could bind and where these binding sites were. The new research answers these fundamental questions and offers potentially practical insights.
This type of surge protection system – which is called photoprotection and has analogues in the plant world – naturally tends to be wasteful. Cyanobacteria are slow to deactivate their photoprotection after doing their job. Now, with a complete picture of how the surge protector works, researchers can design ways to design “smart” and less expensive photoprotection, Kerfeld said.
And, while they help make the planet habitable for humans and countless other organisms that need oxygen to survive, cyanobacteria have a dark side. Cyanobacteria blooms in lakes, ponds and reservoirs can produce toxins that are deadly to native ecosystems as well as humans and their pets. Having a map of how bacteria not only harvest energy from the sun, but also protect themselves from too much of it could inspire new ideas for tackling harmful blooms.
Beyond the new answers and potential applications this work offers, researchers are also excited about the new questions it raises and the research it could inspire.
“If you think of it like Legos, you can keep piling up, right? Proteins and pigments are like blocks that make up the phycobilisome, but then it’s part of the photosystem, which is in the cell membrane, which is part of the whole cell,” Sutter said. “We’re moving up the ladder in a way. We’ve found something new on our ladder, but we can’t say we’ve fixed the system.”
“We answered some questions, but we opened the doors to others and, for me, that’s what makes it a breakthrough,” said Domínguez-Martín. “I’m excited to see how the field develops from here.”
This work was supported by the US Department of Energy’s Office of Science, the National Institutes of Health, the Czech Science Foundation, and the European Union’s Horizon 2020 research and innovation program.