Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature.
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 complexes. 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.
Shlyk-Kerner
Oksana
O
Department of Plant Sciences, The Weizmann Institute of Science, Rehovot 76100, Israel.
Samish
Ilan
I
Kaftan
David
D
Holland
Neta
N
Sai
P S Maruthi
PS
Kless
Hadar
H
Scherz
Avigdor
A
D000064:Acclimatization; D002734:Chlorophyll / Q000378:metabolism; D017124:Conserved Sequence; D000458:Cyanobacteria / Q000737:chemistry / Q000235:genetics / Q000378:metabolism / Q000528:radiation effects; D004583:Electrons; D004735:Energy Transfer; D008958:Models, Molecular; D010788:Photosynthesis / Q000528:radiation effects; D045332:Photosystem II Protein Complex / Q000737:chemistry / Q000378:metabolism; D018583:Pliability; D011487:Protein Conformation; D011506:Proteins / Q000737:chemistry* / Q000378:metabolism*; D020560:Proteobacteria / Q000737:chemistry / Q000378:metabolism / Q000528:radiation effects; D013329:Structure-Activity Relationship; D013696:Temperature
D045332:Photosystem II Protein Complex; D011506:Proteins; D002734:Chlorophyll