Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered Photosystem I complexes
- 117 Downloads
Certain cyanobacteria can thrive in environments enriched in far-red light (700–800 nm) due to an acclimation process known as far-red light photoacclimation (FaRLiP). During FaRLiP, about 8% of the Chl a molecules in the photosystems are replaced by Chl f and a very small amount of Chl d. We investigated the spectroscopic properties of Photosystem I (PSI) complexes isolated from wild-type (WT) Synechococcus sp. PCC 7335 and a chlF mutant strain (lacking Chl f synthase) grown in white and far-red light (WL–PSI and FRL–PSI, respectively). WT–FRL–PSI complexes contain Chl f and Chl a but not Chl d. The light-minus dark difference spectrum of the trapping center at high spectral resolution indicates that the special pair in WT–FRL–PSI consists of Chl a molecules with maximum bleaching at 703–704 nm. The action spectrum for photobleaching of the special pair showed that Chl f molecules absorbing at wavelengths up to 800 nm efficiently transfer energy to the trapping center in FRL–PSI complexes to produce a charge-separated state. This is ~ 50 nm further into the near IR than WL–PSI; Chl f has a quantum yield equivalent to that of Chl a in the antenna, i.e., ~ 1.0. PSI complexes from Synechococcus 7002 carrying 3.8 Chl f molecules could promote photobleaching of the special pair by energy transfer at wavelengths longer than WT PSI complexes. Results from these latter studies are directly relevant to the issue of whether introduction of Chl f synthase into plants could expand the wavelength range available for oxygenic photosynthesis in crop plants.
KeywordsCyanobacteria Photosynthesis Chlorophyll f synthase Action spectrum Quantum yield Far-red light photoacclimation FaRLiP Photosystem I Chlorophyll Cyanobacteria Synechococcus sp. PCC 7002 Synechococcus sp. PCC 7335
This work was supported by the National Science Foundation Grant MCB-1613022 to D.A.B and J.H.G. This research was also conducted under the auspices of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the DOE, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC 0001035 (D.A.B.).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Allakhverdiev SI, Kreslavski VD, Zharmukhamedov SK, Voloshin RA, Korol’kova DV, Tomo T, Shen JR (2016) Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria. Biochemistry (Moscow) 81:201–212Google Scholar
- Bryant DA (2016) Improving crop yields and algal biofuel production by expanding the wavelength range for photosynthesis. Information Systems for Biotechnology News Report pp 1–6Google Scholar
- Cherepanov DA, Shelaev IV, Gostev FE, Mamedov MD, Petrova AA, Aybush AV, Shuvalov VA, Semenov AY, Nadtochenko VA (2017b) Mechanism of adiabatic primary electron transfer in photosystem I: femtosecond spectroscopy upon excitation of reaction center in the far-red edge of the Qy band. Biochim Biophys Acta 1858:895–905CrossRefGoogle Scholar
- Golbeck J (2006) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Springer, DordrechtGoogle Scholar
- Ho M-Y (2018) Characterization of far-red light photoacclimation in cyanobacteria. Biochem Mol Biol 131:173–186Google Scholar
- Hou JM, Boichenko VA, Wang YC, Chitnis PR, Mauzerall D (2001) Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: a pulsed photoacoustic study of electron transfer in photosystem I reveals a similarity to bacterial reaction centers in both volume change and entropy. Biochemistry 40:7109–7116CrossRefGoogle Scholar
- Li Y, Lin Y, Loughlin PC, Chen M (2014) Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris - a filamentous cyanobacterium containing chlorophyll f. Front Plant Sci 5:67Google Scholar
- Miao D, Ding WL, Zhao BQ, Lu L, Xu QZ, Scheer H, Zhao KH (2016) Adapting photosynthesis to the near-infrared: non-covalent binding of phycocyanobilin provides an extreme spectral red-shift to phycobilisome core-membrane linker from Synechococcus sp. PCC 7335. Biochim Biophys Acta 1857:688–694CrossRefGoogle Scholar
- Rippka R, Deuuelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
- Schmitt FJ, Campbell ZY, Bui MV, Huls A, Tomo T, Chen M, Maksimov EG, Allakhverdiev SI, Friedrich T (2018) Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light. Photosynth Res. https://doi.org/10.1007/s11120-11018-10556-11122 Google Scholar
- Shen G, Zhao J, Reimer SK, Antonkine ML, Cai Q, Weiland SM, Golbeck JH, Bryant DA (2002) Assembly of Photosystem I. I. Inactivation of the rubA gene encoding a membrane-associated rubredoxin in the cyanobacterium Synechococcus sp. PCC 7002 causes a loss of Photosystem I activity. J Biol Chem 277:20343–20354CrossRefGoogle Scholar
- Shen G, Schluchter WM, Bryant DA (2008) Biogenesis of phycobiliproteins: I. cpcS-I and cpcU mutants of the cyanobacterium Synechococcus sp. PCC 7002 define a heterodimeric phyococyanobilin lyase specific for beta-phycocyanin and allophycocyanin subunits. J Biol Chem 283:7503–7512CrossRefGoogle Scholar
- Tomo T, Kato Y, Suzuki T, Akimoto S, Okubo T, Noguchi T, Hasegawa K, Tsuchiya T, Tanaka K, Fukuya M, Dohmae N, Watanabe T, Mimuro M (2008) Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J Biol Chem 283:18198–18209CrossRefGoogle Scholar
- Zhao C, Gan F, Shen G, Bryant DA (2015) RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation (FaRLiP). Front Microbiol 6:1303Google Scholar