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Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature

Nature volume 442, pages 827–830 (2006)Cite this article

Abstract

Adjustment of catalytic activity in response to diverse ambient temperatures is fundamental to life on Earth. A crucial example of this is photosynthesis, where solar energy is converted into electrochemical potential that drives oxygen and biomass generation at temperatures ranging from those of frigid Antarctica to those of scalding hot springs. The energy conversion proceeds by concerted mobilization of electrons and protons on photoexcitation of reaction centre protein complexes1,2,3. Following physicochemical paradigms, the rates of imperative steps in this process were predicted to increase exponentially with rising temperatures, resulting in different yields of solar energy conversion at the distinct growth temperatures of photosynthetic mesophiles and extremophiles. In contrast, here we show a meticulous adjustment of energy conversion rate, resulting in similar yields from mesophiles and thermophiles. The key molecular players in the temperature adjustment process consist of a cluster of hitherto unrecognized protein cavities and an adjacent packing motif that jointly impart local flexibility crucial to the reaction centre proteins. Mutations within the packing motif of mesophiles that increase the bulkiness of the amino-acid side chains, and thus reduce the size of the cavities, promote thermophilic behaviour. This novel biomechanical mechanism accounts for the slowing of the catalytic reaction above physiological temperatures in contradiction to the classical Arrhenius paradigm. The mechanism provides new guidelines for manipulating the acclimatization of enzymes to the ambient temperatures of diverse habitats. More generally, it reveals novel protein elements that are of potential significance for modulating structure–activity relationships in membrane and globular proteins alike.

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Figure 1: Conserved structural and functional elements in reaction centres of purple-bacteria and of PSII.
Figure 2: The Q - A → Q B electron transfer rate in mesophilic and thermophilic cyanobacteria.
Figure 3: The effect of D1-212 residues on the PSII reaction centre cavity in T. elongatus structure4.
Figure 4: Temperature dependence and activation parameters of the Q - A → Q B electron transfer in D1-212 mutants of Synechocystis 6803.

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Acknowledgements

We thank B. Loll, J. Biesiadka, and W. Saenger for sending us their PS II reaction centre coordinates before publication; M. Edelman for critical reading of the manuscript; S. Pietrokovski for assistance in data mining sequences; and W. L. DeLano for assistance in applying new PyMol methods. This research was supported by a Sonderforschungsbereich grant and the Willstatter-Avron-Minerva Foundation for Photosynthesis. D.K. was also supported by the Ministry of Education, Youth, and Sports of the Czech Republic; the Academy of Sciences of the Czech Republic; and by the NIH NBCR. A.S. is the incumbent of the Yadelle and Robert Sklare Professorial Chair for Biochemistry. Author Contributions A.S. carried out project planning and supervision. O.S. designed and performed mutagenesis. O.S. and D.K. performed experimental work, mainly at the WIS and partly at USB and ACSR. O.S., D.K. and I.S. performed comparative sequence analysis. I.S. performed the in silico study. O.S., D.K., P.S.M.S., I.S. and A.S. carried out experimental data analysis. H.K. and N.H. helped to establish the mutagenesis program. The study was done in partial fulfilment of the PhD theses of O.S. and I.S.

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Author notes

  1. Ilan Samish

    Present address: Department of Biochemistry and Molecular Biophysics, School of Medicine and Department of Chemistry, School of Arts and Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, 19104, USA

  2. David Kaftan

    Present address: Laboratory of Nanobiology, Institute of Physical Biology USB, and Institute of Systems Biology and Ecology ASCR, Zamek 136, CZ-37333, Nove Hrady, Czech Republic

  3. Neta Holland

    Present address: Department of Biology, Israel Institute of Technology, Haifa, 32000, Israel

  4. P. S. Maruthi Sai

    Present address: Biologics Division, Biological E. Limited 18/1&3, Azamabad, Hyderabad, Andhra Pradesh, 500020, India

  5. Oksana Shlyk-Kerner, Ilan Samish and David Kaftan: *These authors contributed equally to this work

Authors and Affiliations

  1. Department of Plant Sciences, The Weizmann Institute of Science, 76100, Rehovot, Israel

    Oksana Shlyk-Kerner, Ilan Samish, David Kaftan, Neta Holland, P. S. Maruthi Sai, Hadar Kless & Avigdor Scherz

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Shlyk-Kerner, O., Samish, I., Kaftan, D. et al. Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature. Nature 442, 827–830 (2006). https://doi.org/10.1038/nature04947

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