Abstract
Surfactants play a significant role in solubilization of photosystem I (PSI) in vitro. Triton X-100 (TX), n-Dodecyl-β-d-maltoside (DDM), and sodium dodecyl sulfate (SDS) were employed to solubilize PSI particles in MES buffer to compare the effect of surfactant and its dosage on the apparent oxygen consumption rate of PSI. Through a combined assessment of sucrose density gradient centrifugation, Native PAGE and 77 K fluorescence with the apparent oxygen consumption, the nature of the enhancement of the apparent oxygen consumption activity of PSI by surfactants has been analyzed. Aggregated PSI particles can be dispersed by surfactant molecules into micelles, and the apparent oxygen consumption rate is higher for surfactant-solubilized PSI than for integral PSI particles. For DDM, PSI particles are solubilized mostly as the integral trimeric form. For TX, PSI particles are solubilized as incomplete trimeric and some monomeric forms. For the much harsher surfactant, SDS, PSI particles are completely solubilized as monomeric and its subunit forms. The enhancement of the oxygen consumption rate cannot be explained only by the effects of surfactant on the equilibrium between monomeric and trimeric forms of solubililized PSI. Care must be taken when the electron transfer activity of PSI is evaluated by methods based on oxygen consumption because the apparent oxygen consumption rate is influenced by uncoupled chlorophyll (Chl) from PSI, i.e., the larger the amount of uncoupled Chl, the higher the rate of apparent oxygen consumption. 77 K fluorescence spectra can be used to ensure that there is no uncoupled Chl present in the system. In order to eliminate the effect of trace uncoupled Chl, an efficient physical quencher of 1O2, such as 1 mM NaN3, may be added into the mixture.
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Abbreviations
- PSI:
-
Photosystem I
- DDM:
-
n-Dodecyl-β-d-maltoside
- TX:
-
Triton X-100
- SDS:
-
Sodium dodecyl sulfate
- CMC:
-
Critical micelle concentration
- Chl:
-
Chlorophyll
- Chl a :
-
Chlorophyll a
- Phe:
-
Pheophytin
- Phe a :
-
Pheophytin a
- MES:
-
20 mM MES buffer, pH 6.5
- ETC:
-
Electron transfer chain
- DCPIP:
-
2,6-Dichlorophenol indophenol
- MV:
-
Methyl viologen dichloride
- A. platensis :
-
Arthrospira platensis (old name: Spirulina platensis)
References
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55(1):373–399. doi:10.1146/annurev.arplant.55.031903.141701
Bancirova M (2011) Sodium azide as a specific quencher of singlet oxygen during chemiluminescent detection by luminol and Cypridina luciferin analogues. Luminescence 26(6):685–688. doi:10.1002/bio.1296
Chen W, Yang Z-L, Li L-B, Kuang T-Y (2005) Effects of Triton X-100 on the oxygen uptake rate of photosystem I particles treated at 70 °C. J Plant Physiol Mol Biol 31(3):298–304
Chitnis VP, Chitnis PR (1993) PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336(2):330–334. doi:10.1016/0014-5793(93)80831-E
Collini E, Wong CY, Wilk KE, Curmi PMG, Brumer P, Scholes GD (2010) Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463(7281):644–647. doi:10.1038/nature08811
Fischer BB, Hideg É, Krieger-Liszkay A (2013) Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid Redox Signal 18(16):2145–2162. doi:10.1089/ars.2012.5124
Fromme P, Grotjohann I (2006) Structural analysis of cyanobacterial photosystem I. In: Golbeck J (ed) Advances in photosynthesis and respiration, vol 24. Springer, Netherlands, pp 47–69. doi:10.1007/978-1-4020-4256-0_6
Fromme P, Witt HT (1998) Improved isolation and crystallization of photosystem I for structural analysis. Biochim Biophy Acta (BBA) Bioenerg 1365(1–2):175–184. doi:10.1016/S0005-2728(98)00059-0
Giardi MT, Pace E (2005) Photosynthetic proteins for technological applications. Trends Biotechnol 23(5):257–263. doi:10.1016/j.tibtech.2005.03.003
Gunther D, LeBlanc G, Prasai D, Zhang JR, Cliffel DE, Bolotin KI, Jennings GK (2013) Photosystem I on graphene as a highly transparent photoactive electrode. Langmuir 29(13):4177–4180. doi:10.1021/la305020c
Hui Y, Jie W, Carpentier R (2000) Degradation of the photosystem I complex during photoinhibition. Photochem Photobiol 72(4):508–512. doi:10.1562/0031-8655(2000)0720508DOTPIC2.0.CO2
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta (BBA) Bioenerg 1817(1):182–193. doi:10.1016/j.bbabio.2011.04.012
Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411(6840):909–917. doi:10.1038/35082000
Karapetyan NV, Dorra D, Schweitzer G, Bezsmertnaya IN, Holzwarth AR (1997) Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochemistry 36(45):13830–13837. doi:10.1021/bi970386z
Kargul J, Janna Olmos JD, Krupnik T (2012) Structure and function of photosystem I and its application in biomimetic solar-to-fuel systems. J Plant Physiol 169(16):1639–1653. doi:10.1016/j.jplph.2012.05.018
Khorobrykh S, Mubarakshina M, Ivanov B (2004) Photosystem I is not solely responsible for oxygen reduction in isolated thylakoids. Biochim Biophys Acta (BBA) Bioenerg 1657(2–3):164–167. doi:10.1016/j.bbabio.2004.04.009
Kraljić I, Barboy N, Leicknam J-P (1979) Photosensitized formation of singlet oxygen by chlorophyll a in neutral aqueous micellar solutions with Triton X-100. Photochem Photobiol 30(6):631–633. doi:10.1111/j.1751-1097.1979.tb07192.x
Kramarenko GG, Hummel SG, Martin SM, Buettner GR (2006) Ascorbate reacts with singlet oxygen to produce hydrogen peroxide. Photochem photobiol 82(6):1634–1637. doi:10.1111/j.1751-1097.2006.tb09823.x
Krassen H, Schwarze A, Friedrich B, Ataka K, Lenz O, Heberle J (2009) Photosynthetic hydrogen production by a hybrid complex of photosystem I and [NiFe]-hydrogenase. ACS Nano 3(12):4055–4061. doi:10.1021/nn900748j
Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56(411):337–346. doi:10.1093/jxb/erh237
Kruip J, Karapetyan NV, Terekhova IV, Rögner M (1999) In vitro oligomerization of a membrane protein complex: liposome-based reconstitution of trimeric photosystem I from isolated monomers. J Biol Chem 274(26):18181–18188. doi:10.1074/jbc.274.26.18181
Li MY, Cline CS, Koker EB, Carmichael HH, Chignell CF, Bilski P (2001) Quenching of singlet molecular oxygen (1O2) by azide anion in solvent mixtures. Photochem Photobiol 74(6):760–764. doi:10.1562/0031-8655(2001)0740760QOSMOO2.0.CO2
Matsumoto K, Vaughn M, Bruce BD, Koutsopoulos S, Zhang S (2009) Designer peptide surfactants stabilize functional photosystem-I membrane complex in aqueous solution for extended time. J Phys Chem B 113(1):75–83. doi:10.1021/jp8021425
Matsumoto K, Zhang S, Koutsopoulos S (2010) Enhanced electron transfer activity of photosystem I by polycations in aqueous solution. Biomacromolecules 11(11):3152–3157. doi:10.1021/bm100950g
Mukherjee D, May M, Khomami B (2011) Detergent-protein interactions in aqueous buffer suspensions of photosystem I (PS I). J Colloid Interface Sci 358(2):477–484. doi:10.1016/j.jcis.2011.03.070
Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5(12):971–982. doi:10.1038/nrm1525
Ngounou Wetie AG, Sokolowska I, Woods AG, Roy U, Loo JA, Darie CC (2013) Investigation of stable and transient protein–protein interactions: past, present, and future. Proteomics 13(3–4):538–557. doi:10.1002/pmic.201200328
Privé GG (2007) Detergents for the stabilization and crystallization of membrane proteins. Methods 41(4):388–397. doi:10.1016/j.ymeth.2007.01.007
Reisinger V, Eichacker LA (2006) Analysis of membrane protein complexes by blue native PAGE. Proteomics 6(S2):6–15. doi:10.1002/pmic.200600553
Reisinger V, Eichacker LA (2008) Solubilization of membrane protein complexes for blue native PAGE. J Proteomics 71(3):277–283. doi:10.1016/j.jprot.2008.05.004
Reithmeier RAF (2007) Structural biology of membrane proteins. Methods 41(4):353–354. doi:10.1016/j.ymeth.2007.02.016
Rinalducci S, Pedersen JZ, Zolla L (2004) Formation of radicals from singlet oxygen produced during photoinhibition of isolated light-harvesting proteins of photosystem II. Biochim Biophys Acta (BBA) Bioenerg 1608(1):63–73. doi:10.1016/j.bbabio.2003.10.009
Santabarbara S, Bordignon E, Jennings RC, Carbonera D (2002) Chlorophyll triplet states associated with photosystem II of thylakoids. Biochemistry 41(25):8184–8194. doi:10.1021/bi0201163
Schlodder E, Çetin M, Byrdin M, Terekhova IV, Karapetyan NV (2005) P700+- and 3P700-induced quenching of the fluorescence at 760 nm in trimeric photosystem I complexes from the cyanobacterium Arthrospira platensis. Biochim Biophys Acta (BBA) Bioenerg 1706(1–2):53–67. doi:10.1016/j.bbabio.2004.08.009
Scott DJ, Kummer L, Tremmel D, Plückthun A (2013) Stabilizing membrane proteins through protein engineering. Curr Opinin Chem Biol 17(3):427–435. doi:10.1016/j.cbpa.2013.04.002
Sener MK, Park S, Lu D, Damjanovic A, Ritz T, Fromme P, Schulten K (2004) Excitation migration in trimeric cyanobacterial photosystem I. J Chem Phys 120(23):11183–11195. doi:10.1063/1.1739400
Shubin VV, Bezsmertnaya IN, Karapetyan NV (1992) Isolation from Spirulina membranes of two photosystem I-type complexes, one of which contains chlorophyll responsible for the 77 K fluorescence band at 760 nm. FEBS Lett 309(3):340–342. doi:10.1016/0014-5793(92)80803-O
Shubin VV, Tsuprun VL, Bezsmertnaya IN, Karapetyan NV (1993) Trimeric forms of the photosystem I reaction center complex pre-exist in the membranes of the cyanobacterium Spirulina platensis. FEBS Lett 334(1):79–82. doi:10.1016/0014-5793(93)81685-S
Strbac D, Rodrigues M, Santos C, Hall D (1994) Chloroplast isolation from Laminaria digitata (Phaeophyceae): a reproducible methodology yielding photosynthetically active chloroplasts. Planta 195(1):138–141. doi:10.1007/BF00206301
Tamm LK, Liang B (2006) NMR of membrane proteins in solution. Prog Nucl Magn Reson Spectrosc 48(4):201–210. doi:10.1016/j.pnmrs.2006.05.005
Terasaki N, Yamamoto N, Hattori M, Tanigaki N, Hiraga T, Ito K, Konno M, Iwai M, Inoue Y, Uno S, Nakazato K (2009) Photosensor based on an FET utilizing a biocomponent of photosystem I for use in imaging devices. Langmuir 25(19):11969–11974. doi:10.1021/la901091e
Tiwari A, Jajoo A, Bharti S (2008) Heat-induced changes in photosystem I activity as measured with different electron donors in isolated spinach thylakoid membranes. Photochem Photobiol Sci 7(4):485–491. doi:10.1039/B719335A
Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14(4):219–228. doi:10.1016/j.tplants.2009.01.008
Yang Z, Su X, Wu F, Gong Y, Kuang T (2005) Effect of phosphatidylglycerol on molecular organization of photosystem I. Biophys Chem 115(1):19–27. doi:10.1016/j.bpc.2005.01.004
Yu D, Huang F, Xu H (2012) Determination of critical concentrations by synchronous fluorescence spectrometry. Anal Methods 4(1):47–49. doi:10.1039/C1AY05495C
Yu D, Huang G, Xu F, Wang M, Liu S, Huang F (2014) Triton X-100 as an effective surfactant for the isolation and purification of photosystem I from Arthrospira platensis. Photosynth Res 120(3):311–321. doi:10.1007/s11120-014-9988-5
Acknowledgments
We thank Dr. Robert K. Thomas at Oxford University for his critical discussions. The authors appreciate the financial support by the Shandong Provincial Natural Science Foundation (ZR2010BL008), the National Natural Science Foundation of China (21033005, 21073236, 31100263), the program for New Century Excellent Talents in University of Ministry of Education of China (NCET-10-0815), the Natural Science Foundation for Distinguished Young Scholar of Shandong Province (JQ201008), and the Fundamental Research Funds for the Central Universities.
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Yu, D., Huang, G., Xu, F. et al. Effect of surfactants on apparent oxygen consumption of photosystem I isolated from Arthrospira platensis . Photosynth Res 122, 203–213 (2014). https://doi.org/10.1007/s11120-014-0022-8
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DOI: https://doi.org/10.1007/s11120-014-0022-8