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    • 2018-11-05 12:05:42
    • Article ID: 703393

    Researchers create most complete high-res atomic movie of photosynthesis to date

    SLAC's X-ray laser captures the most comprehensive view yet of how plants produce the oxygen we breathe, revealing all four stable states of the process for the first time, and even catching fleeting steps in between. This work is a major step forward in a longstanding quest to 'open a window to the past and unlock the door to a greener future.'

    • Credit: Gregory Stewart/SLAC National Accelerator Laboratory

      Using SLAC’s X-ray laser, researchers have captured the most complete high-res atomic movie to date of Photosystem II, a key protein complex in plants, algae and cyanobacteria responsible for splitting water and producing the oxygen we breathe.

    • Credit: Gregory Stewart/SLAC National Accelerator Laboratory

      In photosystem II, the water-splitting center cycles through four stable states, S0-S3. On a baseball field, S0 would be the start of the game when a batter on home base is ready to hit. S1-S3 would be players waiting on first, second, and third. The center gets bumped up to the next state every time it absorbs a photon of sunlight just like how a player on the field advances one base every time a batter connects with a ball. When the fourth ball is hit, the player slides into home, scoring a run or, in the case of Photosystem II, releasing the oxygen we breathe.

    Menlo Park, Calif. — Despite its role in shaping life as we know it, many aspects of photosynthesis remain a mystery. An international collaboration between scientists at SLAC National Accelerator Laboratory, Lawrence Berkeley National Laboratory and several other institutions is working to change that. The researchers used SLAC’s Linac Coherent Light Source (LCLS) X-ray laser to capture the most complete and highest resolution picture to date of Photosystem II, a key protein complex in plants, algae and cyanobacteria responsible for splitting water and producing the oxygen we breathe. The results were published in Nature today.

    Explosion of life

    When Earth formed about 4.5 billion years ago, the planet’s landscape was almost nothing like what it is today. Junko Yano, one of the authors of the study and a senior scientist at Lawrence Berkeley National Laboratory, describes it as “hellish.” Meteors sizzled through a carbon dioxide-rich atmosphere and volcanoes flooded the surface with magmatic seas.

    Over the next 2.5 billion years, water vapor accumulating in the air started to rain down and form oceans where the very first life appeared in the form of single-celled organisms. But it wasn’t until one of those specks of life mutated and developed the ability to harness light from the sun and turn it into energy, releasing oxygen molecules from water in the process, that Earth started to evolve into the planet it is today. This process, oxygenic photosynthesis, is considered one of nature’s crown jewels and has remained relatively unchanged in the more than 2 billion years since it emerged.

    “This one reaction made us as we are, as the world. Molecule by molecule, the planet was slowly enriched until, about 540 million years ago, it exploded with life,” said co-author Uwe Bergmann, a distinguished staff scientist at SLAC. “When it comes to questions about where we come from, this is one of the biggest.”

    A greener future

    Photosystem II is the workhorse responsible for using sunlight to break water down into its atomic components, unlocking hydrogen and oxygen. Until recently, it had only been possible to measure pieces of this process at extremely low temperatures. In a previous paper, the researchers used a new method to observe two steps of this water-splitting cycle at the temperature at which it occurs in nature.

    Now the team has imaged all four intermediate states of the process at natural temperature and the finest level of detail yet. They also captured, for the first time, transitional moments between two of the states, giving them a sequence of six images of the process.

    The goal of the project, said co-author Jan Kern, a scientist at Berkeley Lab, is to piece together an atomic movie using many frames from the entire process, including the elusive transient state at the end that bonds oxygen atoms from two water molecules to produce oxygen molecules.

    “Studying this system gives us an opportunity to see how metals and proteins work together and how light controls such kinds of reactions,” said Vittal Yachandra, one of the authors of the study and a senior scientist at Lawrence Berkeley National Laboratory who has been working on Photosystem II for more than 35 years. “In addition to opening a window on the past, a better understanding of Photosystem II could unlock the door to a greener future, providing us with inspiration for artificial photosynthetic systems that produce clean and renewable energy from sunlight and water.”

    Sample assembly line

    For their experiments, the researchers grow what Kern described as a “thick green slush” of cyanobacteria — the very same ancient organisms that first developed the ability to photosynthesize — in a large vat that is constantly illuminated. They then harvest the cells for their samples.

    At LCLS, the samples are zapped with ultrafast pulses of X-rays to collect both X-ray crystallography and spectroscopy data to map how electrons flow in the oxygen-evolving complex of photosystem II. In crystallography, researchers use the way a crystal sample scatters X-rays to map its structure; in spectroscopy, they excite the atoms in a material to uncover information about its chemistry. This approach, combined with a new assembly-line sample transportation system, allowed the researchers to narrow down the proposed mechanisms put forward by the research community over the years.

    Mapping the process

    Previously, the researchers were able to determine the room temperature structure of two of the states at a resolution of 2.25 angstroms; one angstrom is about the diameter of a hydrogen atom. This allowed them to see the position of the heavy metal atoms, but left some questions about the exact positions of the lighter atoms, like oxygen. In this paper, they were able to improve the resolution even further, to 2 angstroms, which enabled them to start seeing the position of lighter atoms more clearly, as well as draw a more detailed map of the chemical structure of the metal catalytic center in the complex where water is split.

    This center, called the oxygen-evolving complex, is a cluster of four manganese atoms and one calcium atom bridged with oxygen atoms. It cycles through the four stable oxidation states, S0-S3, when exposed to sunlight. On a baseball field, S0 would be the start of the game when a player on home base is ready to go to bat. S1-S3 would be players on first, second, and third. Every time a batter connects with a ball, or the complex absorbs a photon of sunlight, the player on the field advances one base. When the fourth ball is hit, the player slides into home, scoring a run or, in the case of Photosystem II, releasing breathable oxygen.

    The researchers were able to snap action shots of how the structure of the complex transformed at every base, which would not have been possible without their technique. A second set of data allowed them to map the exact position of the system in each image, confirming that they had in fact imaged the states they were aiming for.

    Sliding into home

    But there are many other things going on throughout this process, as well as moments between states when the player is making a break for the next base, that are a bit harder to catch. One of the most significant aspects of this paper, Yano said, is that they were able to image two moments in between S2 and S3. In upcoming experiments, the researchers hope to use the same technique to image more of these in-between states, including the mad dash for home — the transient state, or S4, where two atoms of oxygen bond together — providing information about the chemistry of the reaction that is vital to mimicking this process in artificial systems.

    “The entire cycle takes nearly two milliseconds to complete,” Kern said. “Our dream is to capture 50 microsecond steps throughout the full cycle, each of them with the highest resolution possible, to create this atomic movie of the entire process.”

    Although they still have a way to go, the researchers said that these results provide a path forward, both in unveiling the mysteries of how photosynthesis works, and in offering a blueprint for artificial sources of renewable energy. 

    “It’s been a learning process,” said SLAC scientist and co-author Roberto Alonso-Mori. “Over the last seven years we’ve worked with our collaborators to reinvent key aspects of our techniques. We’ve been slowly chipping away at this question and these results are a big step forward.”

    In addition to SLAC and Berkeley Lab, the collaboration includes researchers from Umeå University, Uppsala University, Humboldt University of Berlin, the University of California, Berkeley, the University of California, San Franciscoand the Diamond Light Source.

    Key components of this work were carried out at SLAC’s Stanford Synchrotron Radiation Lightsource (SSRL), Berkeley Lab’s Advanced Light Source (APS) and Argonne National Laboratory’s Advanced Photon Source (APS). LCLS, SSRL, APS, and ALS are DOE Office of Science user facilities. This work was supported by the DOE Office of Science and the National Institutes of Health, among other funding agencies.

    SLAC is a multi-program laboratory exploring frontier questions in photon science, astrophysics, particle physics and accelerator research. Located in Menlo Park, California, SLAC is operated by Stanford University for the U.S. Department of Energy Office of Science. To learn more, please visit www.slac.stanford.edu. 

    SLAC National Accelerator Laboratory is supported by the Office of Science of the U.S. Department of Energy. The Office of Science is the single largest supporter of basic research in the physical sciences in the United States, and is working to address some of the most pressing challenges of our time. For more information, please visit science.energy.gov.

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    Microbes Eat the Same in Labs and the Desert

    Analyses of natural communities forming soil crusts agree with laboratory studies of isolated microbe-metabolite relationships.

    Scientists Produce 3-D Chemical Maps of Single Bacteria

    Scientists at the National Synchrotron Light Source II (NSLS-II)--a U.S. Department of Energy (DOE) Office of Science User Facility at DOE's Brookhaven National Laboratory--have used ultrabright x-rays to image single bacteria with higher spatial resolution than ever before. Their work, published in Scientific Reports, demonstrates an x-ray imaging technique, called x-ray fluorescence microscopy (XRF), as an effective approach to produce 3-D images of small biological samples.

    Self-Sensing Materials Are Here

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    Climate Simulations Project Wetter, Windier Hurricanes

    New supercomputer simulations by climate scientists at the Department of Energy's Lawrence Berkeley National Laboratory (Berkeley Lab) have shown that climate change intensified the amount of rainfall in recent hurricanes such as Katrina, Irma, and Maria by 5 to 10 percent. They further found that if those hurricanes were to occur in a future world that is warmer than present, those storms would have even more rainfall and stronger winds.

    Tiny Titanium Barrier Halts Big Problem in Fuel-Producing Solar Cells

    New design coats molecular components and dramatically improves stability under tough, oxidizing conditions.

    X-Rays Show How Periods of Stress Changed an Ice Age Hyena to the Bone

    An international team has unearthed what life might have been like for a now-extinct subspecies of spotted hyena. They found that despite their massive size, some cave hyenas experienced times of hardship that affected them to the bone, causing areas of arrested growth that appear as dark lines, like rings on a tree trunk.

    Turning Wood Scraps into Tape

    A new chemical process converts a component of wasted wood pulp and other biomass into high-value pressure-sensitive adhesives.


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    Argonne's Min Si receives early career award from IEEE Computer Society

    Argonne's Min Si wins Award for Excellence for Early Career Researchers in High Performance Computing through the Institute of Electrical and Electronics Engineers.

    Jefferson Lab Director Appointed to Distinguished Professorship

    Stuart Henderson, director of the Department of Energy's Thomas Jefferson National Accelerator Facility, has been appointed the Governor's Distinguished CEBAF professor at Old Dominion University. The position is supported by the Commonwealth of Virginia and is named for the Continuous Electron Beam Accelerator Facility, which is the main research facility located at Jefferson Lab.

    DOE issues call for HPC for Energy Innovation proposals

    The U.S. Department of Energy's (DOE) High Performance Computing for Energy Innovation (HPC4EI) Initiative today issued its first joint solicitation for the High Performance Computing for Manufacturing Program (HPC4Mfg) and the High Performance Computing for Materials Program (HPC4Mtls).

    DOE funding advances project to turn captured CO2 into key chemicals

    The U.S. Department of Energy has selected Southern Research for an award of up to $1.5 million to advance technology for carbon dioxide utilization.

    Sierra Reaches Higher Altitudes, Takes Number Two Spot on List of Fastest Supercomputers

    Sierra, Lawrence Livermore National Laboratory's newest supercomputer, rose to second place on the list of the world's fastest computing systems, TOP500 List representatives announced Monday at the International Conference for High Performance Computing, Networking, Storage and Analysis conference (SC18) in Dallas.

    Green energy: Wind energy agreement will provide savings, 50 percent of electricity needs for Kansas State University Manhattan campus

    Kansas State University has signed an agreement with Westar Energy to provide approximately 50 percent of the energy needs for the university's main Manhattan campus from a wind farm in Nemaha County and save the university nearly $200,000 annually.

    INCITE grants awarded to 62 computational research projects

    The U.S. Department of Energy announced new projects for 2019 through its Innovative and Novel Computational Impact on Theory and Experiment (INCITE) program.

    Argonne's Raj Kettimuthu Named ACM Distinguished Member

    Argonne computer scientist Raj Kettimuthu recently was named a Distinguished Member of the Association for Computing Machinery for his development of tools to analyze and enhance end-to-end data transfer performance.

    Jefferson Lab-Affiliated Researchers Honored as APS Fellows

    The Department of Energy's Thomas Jefferson National Accelerator Facility now has a few more fellows on campus. The American Physical Society, a professional membership society that works on behalf of the physics community, recently announced its list of 2018 fellowships.

    Jefferson Lab Receives DOE Award for Energy Efficient Upgrade

    On Oct. 23, a team from the Department of Energy's Thomas Jefferson National Accelerator Facility was honored at the 2018 Federal Energy and Water Management Award Ceremony for upgrades made to the lab's data center, ultimately improving its energy efficiency.


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    Microbes Eat the Same in Labs and the Desert

    Analyses of natural communities forming soil crusts agree with laboratory studies of isolated microbe-metabolite relationships.

    Diverse Biofeedstocks Have High Ethanol Yields and Offer Biorefineries Flexibility

    Evidence suggests that biorefineries can accept various feedstocks without negatively impacting the amount of ethanol produced per acre.

    Opening Access to Explore the Synthetic Chemistry of Neptunium

    New, easily prepared starting material opens access to learning more about a difficult-to-control element in nuclear waste.

    Tiny Titanium Barrier Halts Big Problem in Fuel-Producing Solar Cells

    New design coats molecular components and dramatically improves stability under tough, oxidizing conditions.

    Turning Wood Scraps into Tape

    A new chemical process converts a component of wasted wood pulp and other biomass into high-value pressure-sensitive adhesives.

    Very Heavy Elements Deliver More Electrons

    Scientists revise understanding of the limits of bonding for very electron-rich heavy elements.

    Probing Water's "No-Man's Land" Temperature Region

    Measuring the physical properties of water at previously unexplored temperatures offers insights into one of the world's essential liquids.

    Novel Soil Bacteria with Unusual Genes Synthesize Unique Antibiotic Precursors

    A large-scale soil project uncovered genetic information from bacteria with the capacity to make specialized molecules that could lead to new pharmaceuticals.

    Warmer Temperatures Lengthen Growing Season, Increase Plants' Vulnerability to Frost

    Experimental warming treatments show how peatland forests may respond to future environmental change.

    Rising Stars Seek to Learn from the Master: Mother Nature

    A trio of scientists was recognized for their early career successes in uncovering how microbes produce fuel, insights that could change our energy portfolio


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