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Formation of photosystem II reaction centers that work as energy sinks in lichen symbiotic Trebouxiophyceae microalgae

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Abstract

Lichens are poikilohydric symbiotic organisms that can survive in the absence of water. Photosynthesis must be highly regulated in these organisms, which live under continuous desiccation-rehydration cycles, to avoid photooxidative damage. Analysis of chlorophyll a fluorescence induction curves in the lichen microalgae of the Trebouxiophyceae Asterochloris erici and in Trebouxia jamesii (TR1) and Trebouxia sp. (TR9) phycobionts, isolated from the lichen Ramalina farinacea, shows differences with higher plants. In the presence of the photosynthetic electron transport inhibitor DCMU, the kinetics of Q A reduction is related to variable fluorescence by a sigmoidal function that approaches a horizontal asymptote. An excellent fit to these curves was obtained by applying a model based on the following assumptions: (1) after closure, the reaction centers (RCs) can be converted into “energy sink” centers (sRCs); (2) the probability of energy leaving the sRCs is very low or zero and (3) energy is not transferred from the antenna of PSII units with sRCs to other PSII units. The formation of sRCs units is also induced by repetitive light saturating pulses or at the transition from dark to light and probably requires the accumulation of reduced Q A, as well as structural changes in the reaction centers of PSII. This type of energy sink would provide a very efficient way to protect symbiotic microalgae against abrupt changes in light intensity.

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Abbreviations

A:

Antenna

b:

Photosystem II reaction center

B t :

Fraction of closed PSII reaction centers at time t

Chyp :

Constant that determines the degree of curvature of fluorescence induction curves

cl:

Closed RC

DCMU:

3-(3′,4′-dichlorophenyl)-1,1-dimethylurea

E :

Energy influx

F o :

Minimal Chl a fluorescence intensity in dark-adapted samples

F m :

Maximal Chl a fluorescence intensity in dark-adapted samples

F v :

Maximum variable Chl a fluorescence (F v = F m − F o)

F v/F m :

An estimate of the maximal quantum yield of PSII photochemistry

F t :

Fluorescence intensity at time t during exposure of samples to light

φ PSII :

Effective quantum efficiency of PSII photochemistry

J :

Light absorption flux per antenna complex or reaction center

K :

Rate constant for the transformation of closed centers to energy sink centers

op:

Open RC

NPQ:

Non-photochemical quenching of excited state of Chl a

OKJIP:

Reference to the typical shape of a fluorescence induction curve (O, origin; K, J, I, three inflection points that appear successively in the induction curve; P, peak)

PQ:

Plastoquinone

PSI:

Photosystem I

P700:

Reaction center of the PSI

PSII:

Photosystem II

p 2,2 :

Probability of excitation energy transfer between two different antenna systems

p 2,b :

Probability of excitation energy transfer between the antenna and P680

Phe:

Pheophytin

p 2G :

Global probability for excitation energy transfer (“exciton” transfer) from one PSII unit to another

RC:

Reaction center

s:

Energy sink

ROS:

Reactive oxygen species

S m :

Complementary area of the fluorescence transient

S t :

Complementary area of the fluorescence transient at time t

V t :

Relative variable fluorescence at time t (V t = F t − F o/F m − F o)

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Acknowledgments

This study was funded by the Spanish Ministry of Science and Innovation (CGL2009-13429-C02-00), Ministerio de Economía y Competitividad (MINECO CGL2012-40058-C02-01/02), FEDER, the Generalitat Valenciana (PROMETEO 2 2013/021 GVA) and the University of Alcalá/CAM (UAH2011/BIO 001). Mr. Daniel Sheerin has reviwed the English version of this paper. We thank all the 3 reviewers of this paper for their valuable comments since they helped us greatly improve our paper.

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  1. Departamento de Ciencias de la Vida, Universidad de Alcalá, Edificio de Ciencias, Campus externo, 28871, Alcalá de Henares, Madrid, Spain

    Alfredo Guéra & Francisco Gasulla

  2. Botánica, ICBIBE, Facultad de Ciencias Biológicas, Universitat de València, C/Dr. Moliner 50, 46100, Burjassot, Valencia, Spain

    Francisco Gasulla & Eva Barreno

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  1. Alfredo Guéra
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Correspondence to Alfredo Guéra.

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11120_2015_196_MOESM1_ESM.xlsx

Supplementary Fig. 1 Vt vs. time curves for 100 µM DCMU-treated samples (red squares) and Vt normalized to V J (Vt/V J ) vs. time curves for non-DCMU-treated samples (blue diamonds) of TR1 (upper panel), TR9 (middle panel) and Asterochloris erici (lower panel) cells. Vt time courses were first determined in disc cultures after 30 min in darkness (non-DCMU-treated cells), then 500 µl of 100 µM DCMU were added to each culture disc and they were maintained in darkness for 30 min and measured again after this period (DCMU treated cells). The intercept, slope and R2 value for each line are indicated. Results are the mean of 3–5 different samples for each species (XLSX 23 kb)

11120_2015_196_MOESM2_ESM.xlsx

Supplementary Fig. 2 ΔB/Δt vs. Vt curves and ΔS/Δt vs. Vt for TR1 (blue diamonds), TR9 (red squares) and Asterochloris erici (green triangles) DCMU treated (upper panel) or control (lower panel) cells. Samples and treatments are the same as in complementary Fig. 1 (XLSX 28 kb)

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Guéra, A., Gasulla, F. & Barreno, E. Formation of photosystem II reaction centers that work as energy sinks in lichen symbiotic Trebouxiophyceae microalgae. Photosynth Res 128, 15–33 (2016). https://doi.org/10.1007/s11120-015-0196-8

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  • DOI: https://doi.org/10.1007/s11120-015-0196-8

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