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Single-Celled Organisms Shed Light on Neurobiology

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Single-Celled Organisms Shed Light on Neurobiology Halobacteria belong to the archaebacteria. They have a particular preference for extremely saline environments. FOCUS_Optogenetics Single-Celled Organisms Shed Light on Neurobiology The discovery of a visual pigment in the cell membrane of an archaebacterium in the early 1970s is owed solely to a researcher’s curiosity: For three years, the scientific community wouldn’t believe Dieter Oesterhelt. Forty years after his pioneering work at the Max Planck Institute of Biochemistry in Martinsried, bacteriorhodopsin and channelrhodopsin, which stems from a single-celled green alga, are gaining ground as new tools in neurobiology. TEXT CHRISTINA BECK t was an illustrious group that the to revolutionize the neurosciences, per- It was more or less a coincidence that Royal Swedish Academy of Sciences mitting, as it does, the first ever non-in- brought biochemist Dieter Oesterhelt invited to the Lilla Frescativägen in vasive manipulation of neural networks into contact with Halobacterium salina- Stockholm on December 12, 2013. in an organism – from the small nem- rum. But this archaebacterium would Optogenetics was the topic on which atode Caenorhabditis elegans to the eventually become the central research I the Nobel Prize Committee was seeking mouse. Someday, perhaps, even in hu- object of his scientific life for the next information. Among the eleven scien- mans. In other words, a method that 40 years. Oesterhelt had done his doc- tists were two from Max Planck insti- has the potential to win a Nobel Prize. torate in Feodor Lynen’s lab at the Max tutes, as well as two other researchers Planck Institute for Cell Chemistry (lat- who had taken their first steps in this THE DISCOVERY OF THE FIRST er the Max Planck Institute of Biochem- field as young group leaders at Max MICROBIAL RHODOPSIN istry) on a metabolic enzyme, fatty acid Planck. synthase. “A giant particle,” as he says, As early as 1979, the discoverer of But what has since become a popular “whose structure could be decoded only the DNA code, Francis A. Crick, called tool of neuroscientists had its begin- through electron microscopy.” it the greatest challenge in the neuro- nings somewhere else entirely: in a small, This explains why the researcher sciences: to selectively influence a spe- halophilic archaebacterium, Halobacte- went on a sabbatical in 1969, to San cific cell type in the brain and leave rium salinarum. Archaebacteria are the Francisco and Walther Stoeckenius, a the others unchanged. In his lectures, “old-timers” of life. Since the early days renowned expert in the field of elec- he speculated that light could serve as of evolution, these single-celled organ- tron microscopy. Oesterhelt wanted to a control tool – in the form of locally isms have persevered in extreme habi- learn to use this technology in the lab and temporally restricted impulses of tats – in salt lakes, for instance, or hot with him. different colors. volcanic springs – while bacteria and Stoeckenius was interested in the Thirty years later, this vision is be- the eukaryotes were able to develop membrane of the halobacterium be- Photo: POWER AND SYRED/SPL/Agentur Focus coming a reality: optogenetics is poised much more freely. cause, at that time, the molecular struc- 4 | 14 MaxPlanckResearch 19 FOCUS_Optogenetics 1969 After completing his doctorate under Feodor Lynen (right) at the Ludwig-Maximilians-Universität Institute of Biochemistry, and a two-year postdoc phase at the Max Planck Institute for Cell Chemistry, young biochemist Dieter Oesterhelt (left) went on a sabbatical to work with Walther Stoeckenius at the University of California, San Francisco in 1969. There he surprisingly succeeded in detecting a rhodopsin-like protein (bacteriorhodopsin) in the membrane of Halobacterium salinarum. ture of cell membranes was still a sub- membrane using mass spectroscopy. equipment. The Max Planck Institute ject of controversy. “That was the so- No doubt about it: it was retinal. Wal- for Cell Chemistry moved out to Mar- called purple membrane, which is how ther Stoeckenius’ initial reaction, how- tinsried, while Oesterhelt remained in it was known even then. But it was ever, was less than euphoric – he said, the originally shared labs at the Lud- completely unclear what it was,” says quite simply: “That can’t be. That wig-Maximilians-Universität Institute Dieter Oesterhelt. doesn’t exist in prokaryotes.” of Biochemistry. “All I had left was a pH Allen Blaurock, who was likewise in The reviewer for the journal NATURE meter, a water bath and a projector,” he Stoeckenius’ lab at the time, requested likely had a similar view. The submit- says. But this situation proved to be a Oesterhelt’s assistance in preparing his ted publication was rejected with a blessing for the key experiment that samples. Oesterhelt experimented with note saying that the experiments were followed, “because I simply couldn’t do different organic solvents to elute the fine, but the analogy with rhodopsin much more.” lipids from the membrane: “So I ex- was pretty far-fetched. “It was simply Oesterhelt was firmly convinced that tracted the purple membrane with unacceptable to find retinal some- the color change is associated with a chloroform/methanol – and suddenly I where other than in an eye,” con- function, so he worked on reversing it: had a yellow extract,” he recalls. cludes Oesterhelt. So the first publica- “Quite simply, I tried every solvent in Such a change in absorption across tion on bacteriorhodopsin, as the the world.” And then here, too, coinci- an area of nearly 200 nanometers authors had christened their molecule, dence again played a role. Specifically, if seemed quite unusual to the young appeared in 1971 in the journal NATURE I took ether, added salt, and then went biochemist. But Allen Blaurock dis- NEW BIOLOGY. to the window when the Sun was shin- missed it – he had worked on frog ret- ing, the extract suddenly turned bright inas with Maurice Wilkins in London. PHOTOSYNTHESIS INVENTED yellow; in the dark, the color changed Their X-ray experiments required NOT ONCE, BUT TWICE back. That was the desired color change, them to irradiate the frog retina at a but what was behind it? very specific angle. “But if we weren’t Dieter Oesterhelt returned to Munich “I simply placed a pH electrode in careful,” Blaurock told Oesterhelt, “the and – despite serious doubts on the part it,” says Oesterhelt. When the color beam went into the frog’s lovely red of his colleagues there – continued to changed from purple to yellow, protons eye, and suddenly it turned yellow.” work with the bacteriorhodopsin: “It were released, and when the color That was the decisive clue for Diet- seems to me to be quite an unusual changed from yellow to purple, protons er Oesterhelt. He went to the library to thing, and it isn’t there without rea- were taken up. Accordingly, the extract retrieve the data on retinal, the light- son,” he explained to the skeptics. And became acidic in the one case, and al- absorbing pigment in the retina of ver- then the shortage of collaborators was kaline in the other. However, when tebrates, and then analyzed the purple also accompanied by a shortage of such a release and uptake of protons Photo: MPG/Krella 20 MaxPlanckResearch 4 | 14 1973 Environment A few short years later, Oesterhelt was able to show that bacteriorhodopsin is a Cell membrane light-driven proton pump. The uptake of photons – that is, light – causes the membrane extracts to change color from purple to yellow (left). In the Bacterio- membrane, the ion pump, rhodopsin activated by light, transports Intracellular protons out of the interior of ATP fluid synthase the bacteria cell, creating a pro- ton concentration gradient between inside and outside. The energy of the protons flow- ing back in is used for enzymat- ic synthesis of ATP (adenosine triphosphate), the energy currency of the cell (right). » It was simply unacceptable to find retinal somewhere other than in an eye.« takes place in a dense layer, such as a concentration gradient is created be- In the years that followed, bacterio- membrane, it would have to create a tween inside and outside, and an elec- rhodopsin rose to become a model pumping effect. trical potential is built up across the subject in bioenergetics, membrane bi- The young biochemist imagined a membrane. “The process is just like ology and structural biology. Since the proton pump – that is, a molecule that charging a battery,” explains the Max start of the second half of the 1970s, takes up protons from one direction Planck researcher. The energy of the there have been more than a hundred and releases them in the other. Oester- protons flowing back in is used for en- publications on this topic each year. In helt presented this idea to his disserta- zymatic synthesis of ATP (adenosine 1977, Japanese researchers Matsuno- tion supervisor Feodor Lynen. He said triphosphate), the energy currency of Yagi and Mukohata discovered a fur- simply: “I don’t believe it, but I certain- the cell. ther pigment in the purple membrane ly hope that you’re right.” If the mole- of Halobacterium salinarum, but it dif- cule pumps protons, then it should be EVEN MORE LIGHT-SWITCHED fered from bacteriorhodopsin. It was possible to measure a pH change in a MEMBRANE PROTEINS long speculated that this was a light- suspension of bacteria cells. activatable sodium pump. Dieter Oesterhelt set up his pH me- This was in line with the chemiosmot- Oesterhelt had since become Direc- ter in the darkroom to see what would ic hypothesis proposed by Peter D. tor at the Max Planck Institute of Bio- happen when he exposed intact cells. Mitchell back in 1961 – which earned chemistry in Martinsried, and one of He set the pH meter to the highest sen- him the Nobel Prize in Chemistry in his first doctoral students there was sitivity and then turned the light on: 1978 – for which bacteriorhodopsin chemist Peter Hegemann.
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