New Insights into the Mechanism of Uphill Excitation Energy Transfer from Core Antenna to Reaction Center in Purple Photosynthetic Bacteria.

The uphill excitation energy transfer (EET) from the core antenna (LH1) to the reaction center (RC) of purple photosynthetic bacteria was investigated at room temperature by comparing the native LH1-RC from Thermochromatium ( Tch.) tepidum with the hybrid LH1-RC from a mutant strain of Rhodobacter ( Rba.) sphaeroides. The latter protein with chimeric Tch-LH1 and Rba-RC exhibits a substantially larger RC-to-LH1 energy difference (Δ E = 630 cm-1) of 3-fold thermal energy (3 kB T). The spectroscopic and kinetics results are discussed on the basis of the newly reported high-resolution structures of Tch. tepidum LH1-RC, which allow us to propose the existence of a passage formed by LH1 BChls that facilitates the LH1 → RC EET. The semilogarithmic plot of the EET rate against Δ E was found to be linear over a broad range of Δ E, which consolidates the mechanism of thermal activation as promoted by the spectral overlap between the LH1 fluorescence and the special pair absorption of RC.

[1]  Maxim I. Kozlov,et al.  Calculation of the excited states properties of LH1 complex of Thermochromatium tepidum , 2018, J. Comput. Chem..

[2]  C. A. Siebert,et al.  Cryo-EM structure of the Blastochloris viridis LH1–RC complex at 2.9 Å , 2018, Nature.

[3]  Jian-Ren Shen,et al.  Structure of photosynthetic LH1–RC supercomplex at 1.9 Å resolution , 2018, Nature.

[4]  M. Rätsep,et al.  Spectrally Selective Spectroscopy of Native Ca-Containing and Ba-Substituted LH1-RC Core Complexes from Thermochromatium tepidum. , 2017, The journal of physical chemistry. B.

[5]  Cvetelin Vasilev,et al.  Engineering of a calcium-ion binding site into the RC-LH1-PufX complex of Rhodobacter sphaeroides to enable ion-dependent spectral red-shifting , 2017, Biochimica et biophysica acta. Bioenergetics.

[6]  M. Madigan,et al.  Probing structure–function relationships in early events in photosynthesis using a chimeric photocomplex , 2017, Proceedings of the National Academy of Sciences.

[7]  R. van Grondelle,et al.  Temperature dependent LH1→RC energy transfer in purple bacteria Tch. tepidum with shiftable LH1-Qy band: A natural system to investigate thermally activated energy transfer in photosynthesis. , 2016, Biochimica et biophysica acta.

[8]  Z. Wang-Otomo,et al.  Thermal Adaptability of the Light-Harvesting Complex 2 from Thermochromatium tepidum: Temperature-Dependent Excitation Transfer Dynamics. , 2015, The journal of physical chemistry. B.

[9]  K. Miki,et al.  Structure of the LH1–RC complex from Thermochromatium tepidum at 3.0 Å , 2014, Nature.

[10]  V. Shuvalov,et al.  The site-directed mutation I(L177)H in Rhodobacter sphaeroides reaction center affects coordination of P(A) and B(B) bacteriochlorophylls. , 2012, Biochimica et biophysica acta.

[11]  Graham R Fleming,et al.  Lessons from nature about solar light harvesting. , 2011, Nature chemistry.

[12]  Jianping Zhang,et al.  Excitation dynamics of two spectral forms of the core complexes from photosynthetic bacterium Thermochromatium tepidum. , 2008, Biophysical journal.

[13]  Hiroaki Suzuki,et al.  Purification, characterization and crystallization of the core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum. , 2007, Biochimica et biophysica acta.

[14]  Katie E. Evans,et al.  A bacteriophytochrome regulates the synthesis of LH4 complexesin Rhodopseudomonas palustris , 2005, Photosynthesis Research.

[15]  H. Sumi.  Uphill energy trapping by reaction center in bacterial photosynthesis. 2: Unistep charge separation, virtually mediated by special pair, by photoexcitation in place of excitation transfer from the antenna system , 2004 .

[16]  Leonas Valkunas,et al.  Exciton dynamics in ring-like photosynthetic light-harvesting complexes: a hopping model , 2004 .

[17]  N. Isaacs,et al.  Crystal Structure of the RC-LH1 Core Complex from Rhodopseudomonas palustris , 2003, Science.

[18]  H. Sumi.  Uphill Energy Trapping by Reaction Center in Bacterial Photosynthesis: Charge Separation Unistep from Antenna Excitation, Virtually Mediated by Special-Pair Excitation , 2002 .

[19]  N. Isaacs,et al.  The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. , 2001, Biochemistry.

[20]  J. Amesz,et al.  A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm. , 2001, Biochemistry.

[21]  G. Fleming,et al.  Calculation of Couplings and Energy-Transfer Pathways between the Pigments of LH2 by the ab Initio Transition Density Cube Method , 1998 .

[22]  V. Sundström,et al.  Temperature Dependence of Excitation Transfer in LH2 of Rhodobacter sphaeroides , 1997 .

[23]  F. van Mourik,et al.  Trapping kinetics in mutants of the photosynthetic purple bacterium Rhodobacter sphaeroides: influence of the charge separation rate and consequences for the rate-limiting step in the light-harvesting process. , 1994, Biochemistry.

[24]  V. Sundström,et al.  Energy transfer within the isolated B875 light‐harvesting pigment‐protein complex of Rhodobacter sphaeroides at 77 K studied by picosecond absorption spectroscopy , 1988 .

[25]  Robert Eugene Blankenship,et al.  Properties of the reaction center of the thermophilic purple photosynthetic bacterium Chromatium tepidum. , 1987, Biochimica et biophysica acta.

[26]  P. Sebban,et al.  ISOLATION and SPECTROSCOPIC CHARACTERIZATION OF THE B875 ANTENNA COMPLEX OF A MUTANT OF Rhodopseudomonas sphaeroides , 1985 .

[27]  T. G. Monger,et al.  Light collection and harvesting processes in bacterial photosynthesis investigated on a picosecond time scale. , 1977, Proceedings of the National Academy of Sciences of the United States of America.