Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature

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 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.

Characterization of Two Thermostable Cyanobacterial Phytochromes Reveals Global Movements in the Chromophore-binding Domain during Photoconversion

“…Thermostable enzymes typically work more efficiently at higher temperatures, with optimal performance often matching the preferred growth temperature of the host organism (61). This expectation may also hold true for the Pr/Pfr interconversion of SyA-Cph1 and SyB-Cph1.…”

Two Different Charge Separation Pathways in Photosystem II

“…The functional role of the protein matrix has been investigated before: changes in locally flexible domains in type I and II reaction centers have been shown to provide the means for adaptation of the enzyme to the ambient temperature (44), in the photsystem I complex of cyanobacteria protein dynamics have been shown to induce variation in energy transfer pathways (45), and for the bacterial reaction center the role of the protein matrix in controlling the kinetics of initial electron transfer has been demonstrated (46). In the latter contribution, the authors argue that the charge separation kinetics is determined by protein conformational changes induced by the absorption of light.…”

Structural differences between thermophilic and mesophilic membrane proteins

“…18,19 Nevertheless, either increased packing efficiency or increased burial could be an important factor in stabilizing membrane proteins in hot environments. 15 We therefore investigated whether packing density and burial are different in mesophiles and thermophiles.…”

“…They observed a striking depletion of Cys residues in thermophiles and an increase in Gly, Ser, and Ala pair motifs, suggesting a preference for the packing of small residues. By comparing mesophilic and thermophilic reaction center sequences and structures, Shlyk-Kerner et al 15 showed that subtle changes in cavity volumes in photosynthetic reaction centers were a key factor in switching between thermophilic and mesophilic properties, implying an important role for packing in thermal adaptation.…”