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Dynamics and mechanism of a light-driven chloride pump

February 7, 2022

(Published in Science)
Chloride transport by microbial rhodopsins is an essential process for which molecular details—such as the mechanisms that convert light energy to drive ion pumping and ensure the unidirectionality of the transport—have remained elusive. We combined time-resolved serial crystallography with time-resolved spectroscopy and multiscale simulations to elucidate the molecular mechanism of a chloride pumping rhodopsin and the structural dynamics throughout the transport cycle. We traced transient anion binding sites, obtained evidence for how light energy is used in the pumping mechanism, and identified steric and electrostatic molecular gates ensuring unidirectional transport. An interaction with the π-electron system of the retinal supports transient chloride ion binding across a major bottleneck in the transport pathway. These results allow us to propose key mechanistic features enabling finely controlled chloride transport across the cell membrane in this light powered chloride ion pump.


Figure 1. Photoactive chloride pumping through the cell membrane captured by time-resolved serial crystallography: Chloride ions (green spheres) are transported across the cell membrane by the NmHR chloride pump (pink). (Graphic: Guillaume Gotthard, Sandra Mous)

Many bacteria and unicellular algae have light-driven pumps in their cell membranes: proteins that change shape when exposed to photons such that they can transport charged atoms in or out of the cell. Thanks to these pumps, their unicellular owners can adjust to the environment’s pH value or salinity.

One such bacteria is Nonlabens marinus, first discovered in 2012 in the Pacific Ocean. Among others, it possesses a rhodopsin protein in its cell membrane which transports chloride anions from outside the cell to its inside. Just like in the human eye, a retinal molecule bound to the protein isomerizes when exposed to light. This isomerization starts the pumping process. Researchers now gained detailed insight into how the chloride pump in Nonlabens marinus works.

The study was led by Przemyslaw Nogly, once a postdoc at PSI and now an Ambizione Fellow and Group Leader at ETH Zürich. With his team, he combined experiments at two of PSI’s large-scale research facilities, the Swiss Light Source SLS and the X-ray free-electron laser SwissFEL. Slower dynamics in the millisecond-range were investigated via time-resolved serial crystallography at SLS while faster, up to picosecond, events were captured at SwissFEL - then both sets of data were put together.

“In one paper, we exploit the advantages of two state-of-the-art facilities to tell the full story of this chloride pump,” Nogly says. Jörg Standfuss, co-author of the study who built up a PSI team dedicated to creating such molecular movies, adds: “This combination enables first-class biological research as would only be possible at very few other places in the world beside PSI.”


 
Reference: Mous, S., Gotthard, G., Ehrenberg, D., Sen, S., Weinert, T., Johnson Philip, J.M., James, D., Nass, K., Furrer, A., Kekilli, D., Ma, P., Brünle, S., Casadei Cecilia, M., Martiel, I., Dworkowski, F., Gashi, D., Skopintsev, P., Wranik, M., Knopp, G., Panepucci, E., Panneels, V., Cirelli, C., Ozerov, D., Schertler, G., Wang, M., Milne, C., Standfuss, J., Schapiro, I., Heberle, J., and Nogly, P. (2022). Dynamics and mechanism of a light-driven chloride pump. Science, eabj6663 (10.1126/science.abj6663).

See also: PSI news, ,
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