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Model for fluorescence quenching in light harvesting complex II in different aggregation states

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Abstract

Low-temperature (77 K) steady-state fluorescence emission spectroscopy and dynamic light scattering were applied to the main chlorophyll a/b protein light harvesting complex of photosystem II (LHC II) in different aggregation states to elucidate the mechanism of fluorescence quenching within LHC II oligomers. Evidences presented that LHC II oligomers are heterogeneous and consist of large and small particles with different fluorescence yield. At intermediate detergent concentrations the mean size of the small particles is similar to that of trimers, while the size of large particles is comparable to that of aggregated trimers without added detergent. It is suggested that in small particles and trimers the emitter is monomeric chlorophyll, whereas in large aggregates there is also another emitter, which is a poorly fluorescing chlorophyll associate. A model, describing populations of antenna chlorophyll molecules in small and large aggregates in their ground and first singlet excited states, is considered. The model enables us to obtain the ratio of the singlet excited-state lifetimes in small and large particles, the relative amount of chlorophyll molecules in large particles, and the amount of quenchers as a function of the degree of aggregation. These dependencies reveal that the quenching of the chl a fluorescence upon aggregation is due to the formation of large aggregates and the increasing of the amount of chlorophyll molecules forming these aggregates. As a consequence, the amount of quenchers, located in large aggregates, is increased, and their singlet excited-state lifetimes steeply decrease.

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Abbreviations

LHC II:

Main chlorophyll a/b protein light harvesting complex of photosystem II

chl:

Chlorophyll

NPQ:

Non-photochemical quenching

DM:

n-Dodecyl β-d-maltoside

CMC:

Critical micelle concentration

F680:

Fluorescence band at 680 nm

F700:

Fluorescence band at 698 nm

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Acknowledgments

This study was supported by Grant No. 11 (Program “Support for the research activities at the universities”) from the Scientific Research Fund of the Ministry of Education and Science of Bulgaria and by Grant No. 16 from the Scientific Research Foundation at Sofia University, Bulgaria.

Author information

Authors and Affiliations

  1. Department of Condensed Matter Physics, Faculty of Physics, Sofia University, 5, J. Bourchier blvd., 1164, Sofia, Bulgaria

    Atanaska Andreeva, Silvia Abarova & Katerina Stoitchkova

  2. Institute of Biophysics, Bulgarian Academy of Sciences, Acad. G. Bonchev str. bl.21, 1113, Sofia, Bulgaria

    Mira Busheva

Authors
  1. Atanaska Andreeva
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  2. Silvia Abarova
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  3. Katerina Stoitchkova
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  4. Mira Busheva
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Corresponding author

Correspondence to Atanaska Andreeva.

Appendices

Appendix 1: Estimation of the ratio of the rate constants for excitation energy transfer from F680 to F700

It is well documented that the process of excitation energy transfer between the antenna pigments in green plants can be described with the localized Förster mechanism (Van Grondelle et al. 1994; Palacios et al. 2002) and the rate constant for excitation energy transfer is proportional to the minus sixth power of the distance between pigments:

$$ k_{12} = {\text{const}}\;n^{ - 4} \,k^{2} \,R^{ - 6} , $$
(5)

where n is the refraction index, k is the factor for orientation of the molecules and R is the distance between them. It was shown that the average distance between the pigments in trimeric LHC II is 11. 26 Å (Standfuss et al. 2005; Liu et al. 2004), whereas the distance between F680 and F700 is around 14 Å (Standfuss et al. 2005); (Standfuss et al. 2005; Liu et al. 2004). Using Eq. 5 it is easy to calculate that the ratio of the rate constant for energy transfer between F680 and F700 to the average rate constant is 0.14, which enables us to neglect it in a first approximation.

Appendix 2: Evaluation of the rate constant for fluorescence

The rate constant for fluorescence k F is given by:

$$ k_{\text{F}} = \frac{1}{{\tau_{R} }} \approx {\text{const}}\tilde{\nu }_{0}^{2} \,\varepsilon_{\max } \,\Updelta \tilde{\nu }, $$
(6)

where τ R is the chl a fluorescence lifetime, \( \tilde{\nu } \) is the frequency in wavenumbers, \( \Updelta \tilde{\nu } \) is the full width at half maximum, \( \tilde{\nu }_{0} \) is the wavenumber at the absorption maximum and ε max is the extinction coefficient at \( \tilde{\nu }_{0} \). On the basis of the literature data (Shipman et al. 1976) about the values of \( \tilde{\nu }_{0} \) = 15,170 cm−1, \( \Updelta \tilde{\nu } \) = 440 cm−1 and ε max = 84.9 for monomeric chl a and 14,940 cm−1, 720 cm−1 and 55.7, respectively for dimeric chl a, the ratio of their fluorescence rate constants is estimated to be 0.96. Therefore, it is safe to assume that k F is the same for chl monomers and chl dimers.

Appendix 3: Differential equations describing the chl a fluorescence quenching within LHC II with different degree of aggregation at low temperature (77 K)

The model (Fig. 5) leads to the following five differential equations:

$$ \frac{{{\text{d}}n_{{1{\text{T}}}} }}{{{\text{d}}t}} = {{\sigma \;n_{{0{\text{T}}}} I - k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } \mathord{\left/ {\vphantom {{\sigma \;n_{{0{\text{T}}}} I - k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } {N_{0} }}} \right. \kern-\nulldelimiterspace} {N_{0} }} $$
(7)
$$ \frac{{{\text{d}}n_{{2{\text{T}}}} }}{{{\text{d}}t}} = {{k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } \mathord{\left/ {\vphantom {{k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } {N_{0} - \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{T}}}} }}} \right. \kern-\nulldelimiterspace} {N_{0} - \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{T}}}} }} $$
(8)
$$ \frac{{{\text{d}}n_{{1{\text{A}}}} }}{{{\text{d}}t}} = {{{{\sigma \;n_{{0{\text{A}}}} I\; - k_{13} n_{03} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{\sigma \;n_{{0{\text{A}}}} I\; - k_{13} n_{03} n_{{1{\text{A}}}} } {N_{0} }}} \right. \kern-\nulldelimiterspace} {N_{0} }} - k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{{{\sigma \;n_{{0{\text{A}}}} I\; - k_{13} n_{03} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{\sigma \;n_{{0{\text{A}}}} I\; - k_{13} n_{03} n_{{1{\text{A}}}} } {N_{0} }}} \right. \kern-\nulldelimiterspace} {N_{0} }} - k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} } {N_{0} }}} \right. \kern-\nulldelimiterspace} {N_{0} }} $$
(9)
$$ \frac{{{\text{d}}n_{3} }}{{{\text{d}}t}} = {{k_{13} n_{03} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{k_{13} n_{03} n_{{1{\text{A}}}} } {N_{0} - \left( {k{}_{\text{F}} + k_{\text{ic}}^{\text{D}} } \right)n_{3} }}} \right. \kern-\nulldelimiterspace} {N_{0} - \left( {k{}_{\text{F}} + k_{\text{ic}}^{\text{D}} } \right)n_{3} }} $$
(10)
$$ \frac{{{\text{d}}n_{{2{\text{A}}}} }}{{{\text{d}}t}} = {{k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} } {N_{o} - \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{A}}}} ,}}} \right. \kern-\nulldelimiterspace} {N_{o} - \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{A}}}} ,}} $$
(11)

where I is the intensity of excitation light and k ic is the rate constant for internal conversion.

In steady state \( \frac{{{\text{d}}n_{i} }}{{{\text{d}}t}} = 0 \) and the Eqs. 7–11 become:

$$ \sigma \;n_{{0{\text{T}}}} I\; = {{k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } \mathord{\left/ {\vphantom {{k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } {N_{0} }}} \right. \kern-\nulldelimiterspace} {N_{0} }} $$
(7')
$$ {{k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } \mathord{\left/ {\vphantom {{k_{12} n_{{02{\text{T}}}} n_{{1{\text{T}}}} } {N_{0} = \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{T}}}} }}} \right. \kern-\nulldelimiterspace} {N_{0} = \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{T}}}} }} $$
(8')
$$ {{{{\sigma \;n_{{0{\text{A}}}} I = k_{13} n_{03} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{\sigma \;n_{{0{\text{A}}}} I = k_{13} n_{03} n_{{1{\text{A}}}} } {N_{0} + k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} }}} \right. \kern-\nulldelimiterspace} {N_{0} + k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} }}} \mathord{\left/ {\vphantom {{{{\sigma \;n_{{0{\text{A}}}} I = k_{13} n_{03} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{\sigma \;n_{{0{\text{A}}}} I = k_{13} n_{03} n_{{1{\text{A}}}} } {N_{0} + k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} }}} \right. \kern-\nulldelimiterspace} {N_{0} + k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} }}} {N_{0} }}} \right. \kern-\nulldelimiterspace} {N_{0} }} $$
(9')
$$ {{k_{13} n_{03} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{k_{13} n_{03} n_{{1{\text{A}}}} } {N_{0} = \left( {k{}_{\text{F}} + k_{\text{ic}}^{\text{D}} } \right)n_{3} }}} \right. \kern-\nulldelimiterspace} {N_{0} = \left( {k{}_{\text{F}} + k_{\text{ic}}^{\text{D}} } \right)n_{3} }} $$
(10')
$$ {{k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} } \mathord{\left/ {\vphantom {{k_{12} n_{{02{\text{A}}}} n_{{1{\text{A}}}} } {N_{0} = \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{A}}}} }}} \right. \kern-\nulldelimiterspace} {N_{0} = \left( {k_{\text{F}} + k_{\text{ic}}^{\text{M}} } \right)n_{{2{\text{A}}}} }} $$
(11')

At CMC, when all LHCs form trimers and n 0T  = 1, the energy pathways are only realized via scheme shown in Fig. 5a. Therefore, the fluorescence is emitted only by F680. Its integrated fluorescence is denoted as \( n_{{2{\text{T}}}}^{\text{T}} \), where superscript T means that all LHC II form trimers. Its value is easy to obtain from Eqs. 1′ and 7′:

$$ n_{{2{\text{T}}}}^{\text{T}} = \sigma I\tau_{2} ,\quad {\text{where }}\tau_{2} = \frac{1}{{k_{\text{F}} + k_{\text{ic}}^{\text{M}} }}. $$
(12)

At intermediate DM concentrations, the total fluorescence emitted from F680 can be expressed as follows:

$$ n_{2} = n_{{2{\text{T}}}} + n_{{2{\text{A}}}} $$
(13)

Appendix 4: Equation for n 0A

The quadratic equation for the relative amount of chl molecules in their ground states in large aggregates, n 0A, obtained after the replaces using Eqs. 1′, 7′–11′ and Eqs. 2–4 is:

$$ \frac{{n_{{2{\text{T}}}}^{\text{T}} }}{{\tau_{2} }}n_{{0{\text{A}}}}^{2} + \left( {\frac{{n_{2} }}{{\tau_{2} }} - \frac{{2n_{{2{\text{T}}}}^{\text{T}} }}{{\tau_{2} }}} \right)n_{{0{\text{A}}}} + \frac{{n_{3} }}{{\tau_{3} }} = 0 $$
(14)

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Andreeva, A., Abarova, S., Stoitchkova, K. et al. Model for fluorescence quenching in light harvesting complex II in different aggregation states. Eur Biophys J 38, 199–208 (2009). https://doi.org/10.1007/s00249-008-0370-4

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