# Using exogenous quinones as electron carriers from the photosynthetic chain to produce electricity – An “open-ended” photoelectrochemical story starring microalgae?

Adnan Sayegh, Guillaume Longatte, Léna Beauzamy, Eric Labbé, Olivier Buriez, Jérôme Delacotte, Manon Guille-Collignon, Frédéric Lemaître

<figure><img src="image_1.png" /></figure>

## ► To cite this version:

Adnan Sayegh, Guillaume Longatte, Léna Beauzamy, Eric Labbé, Olivier Buriez, et al.. Using exogenous quinones as electron carriers from the photosynthetic chain to produce electricity – An “open-ended” photoelectrochemical story starring microalgae?. Bioelectrochemistry, 2025, 166, pp.109050. 10.1016/j.bioelechem.2025.109050. hal-05223752

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Submitted on 26 Aug 2025

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# Using exogenous quinones as electron carriers from the photosynthetic chain to produce electricity – An “open-ended” photoelectrochemical story starring microalgae? ☆

Adnan Sayegh<sup>a,b</sup>, Guillaume Longatte<sup>a,b,c</sup>, Léna Beauzamy<sup>a,b,2</sup>, Eric Labbé<sup>a</sup>, Olivier Buriez<sup>a</sup>, Jérôme Delacotte<sup>a</sup>, Manon Guille-Collignon<sup>a</sup>, Frédéric Lemaître<sup>a,*</sup>

## ARTICLE INFO

**Keywords:**

Photosynthesis

Quinones

Electrochemistry

Fluorescence

Algae

Photocurrent

## ABSTRACT

Photosynthesis is an important process in Nature that allows the conversion of solar energy into chemical energy. In the current context of research of renewable energies, it could be relevant to divert the electron flow of the photosynthetic chain towards a collecting electrode. In our research group, we have been working for ten years on a strategy involving a suspension of microalgae in the presence of exogenous quinones as redox mediators. The quinone form is thus reduced by the algae under light while the resulting hydroquinone form is oxidized at the collecting electrode surface. In this context, it becomes fundamental to understand how a given quinone affects the photocurrent produced in terms of intensity and stability. The aim of this article is to summarize our main results in this field and to complete them with some unpublished data treatments. Although the structure-activity relationship of the quinones remains to be discovered, these results give an overview of the current questions, the key parameters to consider, being E° and logP, and the future studies to be performed.

## 1. Introduction

Photosynthesis is used by photoautotrophic organisms to transform inorganic elements into organic materials through a complex photo-induced process. The case of oxygenic photosynthesis is the most widely described. Here, under the effect of light, CO₂ (in the presence of water) is converted into sugars and O₂. This global reaction takes place along the photosynthetic chain located in the thylakoid membranes. Two photosystems (PSII and PSI) can capture light via chlorophyll antennae. Their excitation triggers charge separations and a succession of electron transfers (ET) particularly resulting in water oxidation (at the level of the oxygen evolution complex – OEC – in PSII) and an H⁺ gradient that triggers ATP synthase activity and, further downstream, processes leading to CO₂ reduction (Calvin cycle). The whole picture can be described by a redox potential diagram known as the “Z-Scheme”

(Scheme 1).

Given that electrons formally flow along the photosynthetic chain, using photosynthesis as a converter of solar energy could be a judicious approach. This is especially relevant in view of current environmental and energy issues, as the substantial energy losses during photosynthesis (yield of only a few %) point to a reservoir that could be harnessed if this electrical energy could be diverted [1,2]. This obviously raises the question of how to harvest this electron flow, and even more so of the limitations of such a process [3].

To date, many strategies have been implemented to use photosynthesis to convert light energy into electricity. In this context, some excellent reviews have presented a particularly well-documented and comprehensive summary of this scientific field [4–7]. Of note, several important trends can be identified from these reviews.

Firstly, the experimental configuration is not necessarily unique.

<footnote><sup>a</sup> Laboratoire Chimie Physique et Chimie du Vivant – CPCV, UMR8228, Département de Chimie, Ecole Normale Supérieure, PSL University, Sorbonne Université, CNRS, Paris 75005, France</footnote>

<footnote><sup>b</sup> Laboratory of Membrane and Molecular Physiology at IBPC, UMR 7141, CNRS/Sorbonne Université, 13 rue Pierre et Marie Curie, 75005 Paris, France</footnote>

<footnote><sup>c</sup> University of Bordeaux, Bordeaux INP, ISM, UMR CNRS 5255, Pessac 33607, France¹</footnote>

<footnote>* This article is part of a Special issue entitled: 'GFB symposium 2025' published in Bioelectrochemistry.</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: frederic.lemaitre@sorbonne-universite.fr (F. Lemaître).</footnote>

<footnote n="1">¹ Present address.</footnote>

<footnote n="2">² Léna Beauzamy deceased in March 2022 before completion of the final version of this manuscript. Her coauthors dedicate this work to her memory</footnote>
Indeed, while it seems obvious that a collecting electrode is required (an anode, since electron extraction results in a final oxidation process) for interacting with the photosynthetic target, the experimental set-up can be either in the form of a half-cell (in a 3-electrode set-up, a potential is imposed on the (working) collecting electrode, and the corresponding current is measured) or in the form of a full cell (the anode compartment is associated with the relevant cathode compartment, and the spontaneous output voltage is measured as a function of the outgoing current) [8]. From a vocabulary point of view, the term “bio-photoelectrochemical system” may be used for general purposes, but the often-used term “biophotovoltaic” especially covers a 2-electrode configuration with a whole photosynthetic organism at the anode. In any case, questions arise about how to compare performance in terms of the electrochemical system being studied (electrochemical cell under forced vs. spontaneous mode of operation, type of electrodes), but also in terms of quantitative criteria (photocurrent vs. power densities) which may or may not be related to illumination (external quantum efficiency, turnover frequency, etc.) and which may be highly time-dependent [6,9–11].

The fact that this point is finally not completely homogenized means that comparisons are reliable within the same study or even between studies in similar configurations. Thus, there are several photosynthetic targets ranging from the simplest to the most complex in terms of Biology [12]. As “parts” of photosynthesis, isolated photosystems (PSII or PSI or even just the Light Harvesting Complex - Reaction Center association), [11,13–16] isolated thylakoids [17] or chloroplasts can be considered. Because these targets cannot be cultured, complete photosynthetic organisms can be used [6,18–20]. The most widely used to date are cyanobacteria (e.g. *Synechocystis* sp. PCC 6803) and microalgae (e.g. *Chlamydomonas reinhardtii*), which perform oxygenic photosynthesis. Purple bacteria (*Rhodobacter capsulatus*, *Rhodobacter sphaeroides*...), somewhat simpler systems that perform anoxygenic photosynthesis, represent a more recent trend [21].

Irrespective of the selected photosynthetic object/system, a further question arises with respect to the efficiency of photosynthetic electron

diverting, i.e. the efficiency of electron transfer to the surface of the collecting electrode [22]. Accordingly, systems that are “mediator-free” or exoelectrogenic can be considered, or those in which a redox mediator is added [7,23,24]. In this case, the mediator acts as an electron carrier, since it is reduced by the photosynthetic target and oxidized at the electrode. It may be in soluble form or as a polymer grafted to the collecting electrode [25]. Obviously, the efficiency issue is also related to the experimental conditions of the biological object, i.e. in suspension or deposited on the working electrode surface [5].

The best performances are obtained with the most straightforward photoconverters such as isolated, electrode-grafted PSIs in the presence of redox mediators [13]. However, the system degrades in the very short term, making these best performances a peak rather than a stable power output [5]. This is why the use of whole organisms seems to be preferable since they can be grown and have the means to repair themselves. This raises the question of the choice of the mediator which must be able to collect photosynthetic electrons without causing deleterious effects on living organisms.

Over the last ten years, our research group has focused on the exploration and selection of quinones as mediators to extract electrons from the photosynthetic chain of the microalgae *Chlamydomonas reinhardtii* in suspension. As discussed below, in the context of photosynthetic electron harvesting by exogenous quinones, the main extraction sites are identified at the PSII level (Scheme 1 and figures below) and in connection with the Q~B~ pocket [26,27]. This is a site close to an embedded quinone, Q~A~. Once reduced to Q~A~, an endogenous plastooquinone molecule (noted PQ) can then enter the pocket to be reduced in fine to plastoquinol PQH~2~. An exogenous quinone can therefore either be reduced by Q~A~ when inserted into the Q~B~ pocket, or reduced by PQH~2~ within the membrane. Unfortunately, the success of the electron harvesting by quinones is not that simple and using exogenous quinones raises many questions we tried to address in the past years. However, the purpose of this article is not to present a comprehensive review of our past work, but rather to report a summary of the most significant results and complementary data treatments. Through the trends highlighted,

<figure><img src="image_3.png" /><figcaption>**Scheme 1.** Z-Scheme describing the different steps involved during oxygenic photosynthesis.</figcaption></figure>
the aim is to identify the questions that need to be addressed and
answered in order to select the most favorable structure for the quinone
as a redox mediator.

## 2. Photocurrent measurements and quinone screening

### 2.1. Electrochemical device for photocurrent monitoring – evidence of electron harvesting by chloroquinones

In order to easily monitor photocurrents from the microalgae/
quinone mixture, a small-volume (500 µL) electrochemical device was
developed, based on a centimeter-sized PDMS well adhered to a gold-
coated ITO electrode (Fig. 1). This enables chronoamperometry mea-
surements of the activity of a suspension of microalgae in the presence of
quinones and under illumination [28]. Unlike the first devices designed
by our research group, [29] stabilization of the baseline current requires
considerably less time, which allow experiments to proceed within
reasonable timescales (around 30 min). Experiments can then be
repeated while varying the experimental parameters and especially the
nature or the concentration of the quinone Q. The applied potential is
chosen to be sufficiently high to allow oxidation of the hydroquinone
form QH₂.

From a given chronoamperogram, it is straightforward to derive the
performance of the system in terms of maximum photocurrent, but also
through the stability of this performance (duration during which the

<figure><img src="image_4.png" /><figcaption>**Fig. 1.** (A) Schematic view of the experimental set-up for chronoamperometry measurements. (B) Usual recorded chronoamperogram from a quinone/microalgae mixture where a current is triggered once turning light on. The three main values being extracted are the maximum photocurrent ($I_{max}$), the steady state duration and the decreasing slope of the unstable photocurrent.</figcaption></figure>

maximum current is stable, rate of current decay) [30]. It is important to
note here that these studies were conducted over relatively short periods
of time (less than an hour) and therefore on microalgae populations that
did not have time to adapt to the presence of quinones over the long
term. Furthermore, the photocurrent obtained in chronoamperometry is
consistent with an electrocatalytic scheme in which Q quinones are
uptaken by algae and then reduced by light-driven photosynthetic
chains. This reduction produces QH₂ hydroquinones, which are then
released and oxidized to quinones at the surface of the collecting elec-
trode. This mechanism is supported by complementary cyclic voltam-
metry experiments (Fig. 2) involving dichloroquinones (see structures in
Scheme 2).

Thus, in the presence of microalgae under dark conditions, 2,5-
dichlorohydroquinone (2,5-DCBQH₂) exhibits the expected voltammo-
gram (Fig. 2A) with the experimental set-up described above in PBS
medium (pH 7.4), i.e. an oxidation forward peak (2,5-DCBQH₂ → 2,5-
DCBQ) and a reduction backward peak (2,5-DCBQ → 2,5-DCBQH₂) of

<figure><img src="image_5.png" /><figcaption>**Fig. 2.** (A) Cyclic voltammogram ($v = 1$ mV s⁻¹) of a 2,5-DCBQH₂ (100 µmol L⁻¹)/WT *Chlamydomonas reinhardtii* (2 10⁷ cells mL⁻¹) mixture under dark or white light conditions. Starting potential = -0.2 V vs Ag/AgCl. (B) Cyclic voltammogram ($v = 100$ mV s⁻¹) of a 2,6-DCBQ (100 µmol L⁻¹)/WT *Chlamydomonas reinhardtii* (2 10⁷ cells mL⁻¹) mixture under dark or white light conditions. Starting potential = 0.35 V vs Ag/AgCl. Electrochemical measurements were performed with the 3-electrodes well set-up (WE = ITO-Au; CE = Pt; REF = Ag/AgCl wire). Adapted from reference [28].</figcaption></figure>
<figure><img src="image_6.png" /><figcaption>With EDGs ("low" redox potential)</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>"Unclassifiable" quinones (redox potential vs substitution)</figcaption></figure>

<figure><img src="image_8.png" /><figcaption>**Scheme 2.** Chemical structures and redox potentials of the quinones considered in this work.</figcaption></figure>

similar magnitude. With a sufficiently low experimental time (v = 1 mV s⁻¹, i.e. ~10 min) and under white light illumination, the backward peak disappears, along with an amplification of the oxidation current. This is in agreement with the recovery of the hydroquinone form resulting from a reaction between excited algae and quinones. Furthermore, and still using the same device, 2,6-dichlorobenzoquinone (2,6-DCBQ) shows the same type of voltammogram (Fig. 2B) in the presence of microalgae in the dark, i.e. a forward peak of reduction (2,6-DCBQ → 2,6-DCBQH₂) and reverse oxidation peak (2,6-DCBQH₂ → 2,6-DCBQ). Once the light is switched on, the peak corresponding to the 2,6-DCBQ signal decreases, while the peak related to 2,6-DCBQH₂ remains

unchanged, indicating conversion of 2,6-DCBQ to 2,6-DCBQH₂ in solution. Taking into account the relatively short timescale of this experiment (100 mV s⁻¹, i.e. ~6 s), this illustrates the fast reactivity and evolution of the algae/quinone system once illumination is triggered.

## 2.2. Extension to other quinones – analysis of chronoamperogram shape

In this context, different quinones were considered with a wide range of redox properties (Scheme 2 including the order of magnitude of the apparent standard potentials for the QH₂/Q at pH 7 and Q⁻/Q; see below). First of all, mono- or disubstituted quinones were studied in
order to highlight the possible effect of electron-donating or electron-withdrawing groups (EDGs or EWGs respectively) and therefore directly the effect of the redox potential of the quinones. In addition, more specific quinones were also investigated, i.e. low or highly hindered quinones, sometimes with a combination of electron-donating and electron-withdrawing groups.

The oxidizing ability of a quinone can be evaluated by the corresponding standard potential. Two redox couples can be thus considered, namely the semiquinone/quinone ($Q^{-}/Q$; $Q^{-} = Q + e^{-}$) or the hydroquinone/quinone ($QH_{2}/Q$; $QH_{2} = Q + 2e^{-} + 2H^{+}$) couples. As the $QH_{2}/Q$ couple involves protons, its apparent value at pH 7, noted $E^{\circ}(QH_{2}/Q)$, will be used. The values used in this article ($E^{\circ}(Q^{-}/Q)$ and $E^{\circ}(QH_{2}/Q)$) are taken from reference [30].

For $C_{Q} = 100 \mu mol L^{-1}$, a reasonable correlation (Fig. 3) can be observed between the value of the maximum photocurrent and the formal standard potential (at pH 7) of the respective quinones ($R^{2} \sim 0.75$). This correlation is independent of the nature of the selected potential, whether for the hydroquinone/quinone couple or the semiquinone/quinone couple. This result is somewhat surprising since it was shown a few years ago that considering the semiquinone/quinone

couple provided a better correlation in a system involving photosynthetic purple bacteria deposited on a Toray carbon paper electrode [31]. This result makes sense, since the reduction of $Q$ by the photosynthetic chain necessarily involves a first step of monoelectronic reduction of quinone to semiquinone. In our case, this suggests that this first electron transfer step would not be limiting within the photosynthetic electron harvesting pathway under our conditions where photosynthetic organisms are in suspension.

Finally, only 1,4-benzoquinone (BQ, 8) appears to differ from this general behavior, i.e. despite a relatively high redox potential, the photocurrent produced from microalgae is close to zero. This suggests that this quinone has additional parallel properties and interactions beyond its photosynthetic electron diverting action. These possible side effects (Michael reaction, toxicity) will be discussed below. In any case, this correlation shows that the most oxidizing quinones, i.e. electron accepting quinones with a significantly positive $E^{\circ}$, drastically increase the photocurrent magnitude. This therefore raises the question of the stability of photocurrents over time.

Photocurrent stability is investigated through two different observables (Fig. 4): the time during which the maximum photocurrent reaches

<figure><img src="image_9.png" /><figcaption>**Fig. 3.** Experimental maximum photocurrents (from a quinone – 100 µmol $L^{-1}$/WT microalgae aqueous mixture – 2 $10^{7}$ cells $mL^{-1}$) measured with the ITO-Au well set-up as a function of standard potentials involving the quinone form. (A) Hydroquinone/quinone redox couple at pH 7. (B) Semiquinone/quinone redox couple. Adapted from reference [30].</figcaption></figure>

<figure><img src="image_10.png" /><figcaption>**Fig. 4.** Experimental maximum photocurrents (from a quinone – 100 µmol $L^{-1}$/WT microalgae aqueous mixture – 2 $10^{7}$ cells $mL^{-1}$) measured with the ITO-Au well set-up as a function of the stability of the signal (top: steady state duration; bottom: photocurrent decreasing rate). BQ (8) is not mentioned as no photocurrent is obtained in the presence of this quinone. Adapted from reference [30].</figcaption></figure>
a quasi-steady state, and the decrease rate of the current once it is no longer stable (this decrease is globally linear). Once again, a clear correlation is found between these two parameters and the maximum photocurrent reached. Given that I<sub>max</sub> reflects the oxidizing power of quinones, it appears that the most rerouting quinones (increase in I<sub>max</sub>) lead to the most transient behaviors (decrease in current stability and high decreasing slope).

Indeed, the most efficient quinones in terms of photosynthetic electron diverting exhibit photocurrent peaks rather than plateaus. This is consistent with side effects of quinones involving either their high oxidizing power or the fact that they are moderately hindered (because they are disubstituted). In other words, quinones can have a poisoning effect. Such an effect is probably not the only reason for the decrease in current (the question of the stability of a given quinone in solution may also be raised, see below) but it can be quantified by means of cell proliferation experiments. They thus help to identify the concentration of quinone that would impair the ability of microalgae to grow under cell culture conditions. A first critical concentration, CC80, is then defined, i.e. the threshold where 20 % of cells still grow.

These CC80 values are then compared with the maximum photo-
current obtained for a quinone concentration of 100 µmol L⁻¹ (Fig. 5).
Importantly, the Iₘₐₓ value is related to the capacity of a quinone to
harvest photosynthetic electrons, and its value is again accurately
correlated with the CC80 values of each quinone. In other words, the
most oxidizing quinones, such as DCBQs (1 and 2) or PPBQ (3), corre-
spond to low CC80 values, i.e. to pronounced toxic and anti-proliferative
behavior. Since the Iₘₐₓ values follow those of both E° and toxic con-
centrations, this suggests that *standard potentials involving quinones may
also be a parameter expressing the possible toxicity of quinones*.

However, the concentration used for chronoamperometry experi-
ments (i.e. 100 µmol L⁻¹) may be either close to or far from the con-
centration values for which an anti-proliferative action occurs. This can
therefore distort comparisons and analyses. This is why a new critical
concentration, CC20, has been defined, at which 80 % of cells still grow.
This is a low-toxicity concentration, corresponding overall to the highest
"friendly" quinone concentration. It is then compared with the
maximum photocurrent measured for this same concentration (Fig. 6).

This new comparison does not necessarily lead to a correlation, but
rather reveals the intrinsic capacity of a given quinone to extract and
produce an electric current from the photosynthetic chain of microalgae.
The maximum photocurrent under these non-toxic conditions can be

<figure><img src="image_11.png" /><figcaption>**Fig. 5.** Experimental maximum photocurrents (from a quinone – 100 µmol L⁻¹/WT microalgae aqueous mixture – 2 10⁷ cells mL⁻¹) measured with the ITO-Au well set-up as a function of the quinone concentration (CC80) where 80 % of microalgae could no longer grow. CC80 was not determined for NBQ (9). Adapted from reference [30].</figcaption></figure>

<figure><img src="image_12.png" /><figcaption>**Fig. 6.** Experimental maximum and stable photocurrents from a quinone (at the "most friendly" concentration, i.e. CC20) and a WT microalgae aqueous mixture (2 10⁷ cells mL⁻¹) measured with the ITO-Au well set-up. CC20 was not determined for NBQ (9). Adapted from reference [30].</figcaption></figure>

divided into two categories. The first category (near-zero I<sub>max</sub> and high CC20 value) corresponds to quinones that weakly acts as harvesting molecules and whose redox potential, apart from BQ (8), is otherwise low. The second, and probably more interesting, category includes quinones which all have a similar maximum photocurrent value (around 4–6 µA), which is stable over time, but with radically different CC20 values.

This shows that there is a “sliding” effect and that quinones with
significantly positive redox potential values lead to similar perfor-
mances when the concentration is adapted. In other words, a quinone
with a high redox potential at a low concentration will give a similar
result to a quinone with a moderate redox potential at a higher con-
centration. This suggests that the trends resulting from the E° or E' analysis
can be modulated by the added quinone concentration value. In this respect,
the optimal performance zone refers to the highest possible photocur-
rent and CC20 values. All in all, DMPPBQ (10) is the quinone with the
best properties to date, with a trisubstituted structure combining EDGs
(methyl) and EWGs (phenyl).

In conclusion, redox potentials are appropriate a priori parameters for selecting a quinone, but this must be counterbalanced by the toxicity problems associated with the concentration used. Furthermore, E° is a thermodynamic parameter related to electron transfer from reduced Q<sub>A</sub> or the pool of reduced plastoquinones. Its relevance is therefore valid, provided that electron transfer remains fast and that the quinone concentration remains sufficiently high so that no mass transfer (MT) limitation occurs (see below). All in all, photocurrent is obviously a key parameter for characterizing and understanding the role of quinones in the photosynthetic electron extraction process. However, it also represents a complex overall global cycling redox sequence involving several steps, and particularly the reduction of the quinone by the photosynthetic chain. It is therefore necessary to study the algae-quinone interactions involved separately by fluorescence means.

**3. Fluorescence measurements**

We have shown that interactions between algae and exodogenous
quinones can be investigated by analyzing the electrochemical signal of
quinones (vide supra) using cyclic voltammetry. Another way of moni-
toring the diverting of electrons is to quantify the light emitted along the
photosynthetic chain in the presence of quinones since fluorescence
emission from chlorophyll antennae at PSII is a competitive pathway for
photosynthetic activity (Fig. 7A). In other words, following excitation of
<figure><img src="image_13.png" /><figcaption>Fig. 7. (A) Schematic view of the PSII evolution after light irradiance in presence of exogenous quinones (noted Q - endogenous quinones, i.e. plastoquinones are referred to PQ). After being excited, PSII can emit fluorescence or evolve towards a reduced state. Competition (dashed lines) thus occurs between fluorescence emission and electron transfer by means of endogenous or exogenous quinones. For more clarity, the possible fluorescence quenching by exogenous quinones (see text about non photochemical quenching) is not shown. (B) Fluorescence levels along a usual fluorescence induction measurement.</figcaption></figure>

the chlorophyll antennae, the exciton can be transferred to P680 and induce reduction of the embedded quinone QA within PSII. The electron harvesting at the level of the reduced PSII (via QA) by exogenous quinones is therefore expected to reduce the level of fluorescence emitted, by shortening the exciton residence time at the antennae.

### 3.1. Defining an appropriate criterion from fluorescence measurements

The ability of a quinone to accept electrons at PSII can therefore be quantified by measuring different levels of fluorescence depending on the selected illumination (Fig. 7B). Considering red actinic light to trigger photosynthetic activity, this gives access from the initial fluorescence F0 to the steady-state fluorescence Fstat. However, to determine a yield, a reference value is needed, which can be obtained with a supersaturating pulse. This reduces all PSII redox sites and prevents any electron transfer to the plastoquinone pool or an exogenous quinone. The corresponding fluorescence level, Fmax, reflects a situation where the PSII capability to convert a photon into an electron is zero.

The PSII fluorescence yield can therefore be defined as:

$$Y(II) = \frac{F_{\max} - F_{\text{stat}}}{F_{\max}} \qquad (1)$$

Y(II) corresponds to the percentage of incident photons converted into electrons along the photosynthetic chain. This value is a priori a

relevant parameter for analyzing the effect of quinones, since it should increase due to the oxidizing action of exogenous quinones. In fact, the analysis is not so simple, as quinones can interact directly with chlorophyll antennae and cause fluorescence quenching, not facilitating electron extraction at the PSII site, but preventing exciton transmission at P680 level. This phenomenon is known as non-photochemical quenching (NPQ), and indeed affects the value of Y(II). For this reason, another yield expression is considered that quantifies the proportion of open and closed centers. A center is open (Scheme 3) when the embedded quinone is in its oxidized form (QA) and closed in its reduced form (QA). Any sufficiently oxidizing exogenous quinone should therefore increase the percentage of open centers. In practice, this percentage, noted qP, is deduced from the fact that the steady state fluorescence (Fstat) is a linear combination of the fluorescence emitted from open (qP × F0) and closed centers ((1 - qP) × Fmax), and is calculated according to the formula:

$$qP = \frac{F_{\max} - F_{\text{stat}}}{F_{\max} - F_{0}} \qquad (2)$$

The interest of qP is dual. Indeed, it is not only an electron extraction efficiency at the PSII output, but it is also unaffected by NPQ.

### 3.2. Main results from qP = f(CQ) curves

For three quinones (2,6-DCBQ, PPBQ and 2,6-DMBQ, i.e. 2, 3 and 5), the effect on ΔpetA mutant algae (where the QA charge cannot be delivered to the b6f complex) shows that the fraction of open centers globally increases as a function of quinone concentration (Fig. 8) [32,33].

Three zones of interest can be more particularly identified on the qP = f(CQ) curves (Fig. 8). Within zone 1 (low concentrations), no effect is observed. At moderate concentrations (zone 2), the percentage of open centers increases as expected, then remains stable at higher concentrations (zone 3).

Indeed, Q can be reduced into QH2 by two main pathways once uptaken by microalgae (i.e. after crossing the cell/chloroplast membranes to access the thylakoid membranes). The first pathway corresponds to electron transfers from reduced QA according to:

$$ \begin{aligned} P_{680} - \text{Pheo} - Q_{A}^{-} + Q &= P_{680} - \text{Pheo} - Q_{A} + Q^{-} \\ P_{680} - \text{Pheo} - Q_{A}^{-} + Q^{-} &= P_{680} - \text{Pheo} - Q_{A} + Q^{2-} \\ Q^{2-} + 2H^{+} &= QH_{2} \end{aligned} $$

A second pathway for exogenous quinones is to interact with the plastoquinone pool (PQ/PQH2) which acts as an endogenous redox carrier from reduced QA.

$$ \begin{aligned} 2P_{680} - \text{Pheo} - Q_{A}^{-} + PQ + 2H^{+} &= 2P_{680} - \text{Pheo} - Q_{A} + PQH_{2} \\ PQH_{2} + Q &= PQ + QH_{2} \end{aligned} $$

Regardless the actual extraction site, zones 2 and 3 are representative

<figure><img src="image_14.png" /><figcaption>Scheme 3. Overall scheme summarizing the path of a photon (“hv”) collected by chlorophyll antennae and their subsequent excitation (*). Only sites related to the text (Chl, P680, embedded quinone QA) are shown for clarity. F corresponds to a fluorescence emission and Q/PQ are the exogenous quinones or the plastoquinone pool respectively.</figcaption></figure>
<figure><img src="image_15.png" /><figcaption>Fig. 10. Experimental NPQ as a function of the added quinone concentration (CQ) for an aqueous mixture of ΔPetA Chlamydomonas reinhardtii microalgae (2 10⁷ cells mL⁻¹) and quinone (2,6-DCBQ, 2). The blue line corresponds to a fitting by considering a loss of quinones. The red line displays a fitting with a maximum and constant loss of quinones. Adapted from reference [32]. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)</figcaption></figure>

$$ 
\left. 
\begin{array}{l}
P' = \frac{C_{Q,lost}}{C_{Q,available}} \\
NPQ = K_{SV}C_{Q,available} \\
C_Q = C_{Q,lost} + C_{Q,available}
\end{array}
\right\} \text{NPQ} = \frac{K_{SV}}{1 + P'} C_Q \qquad (5) 
$$

In the second case, the membranes/compartments are saturated with quinones, allowing us to establish a concentration Csat of lost/unavailable quinones, the excess being available for NPQ. Both situations enable the NPQ = f(CQ) relationship to be predicted, and are experimentally validated. This makes it possible to extract KSV, P' and Csat values for different quinones.

$$ 
\left. 
\begin{array}{l}
C_{sat} = \frac{n_{Q,lost,max}}{V_{total}} \\
C_Q = C_{Q,available} + C_{sat} \\
NPQ = K_{SV}(C_Q - C_{sat}) \\
NPQ = K_{SV}C_{Q,available}
\end{array}
\right\} \text{NPQ} = K_{SV}(C_Q - C_{sat}) \qquad (6) 
$$

It is worth noting that knowing the parameters P' and Csat also enables us to correct the curves qP = f(CQ) by changing the concentration of quinone added in solution to that actually available. The resulting curve makes zone 1 disappear and can be modeled by a Michaelis-Menten type equation, perfectly in line with the extraction mechanism combining charge and mass transfer [33]. While beyond the scope of this work, it is important to know that the calculation of the open center percentage actually depends on the mechanism of light capture by the chlorophyll antennae. This may involve independent centers (a photon is captured either by a center that is either open or closed – “Puddle” mechanism – proportion of open centers noted qP) or connected centers (a photon will always be transferred to an open center regardless of which antenna captures it – “Lake” mechanism – proportion of open centers noted qL) [34]. Consequently, the open center fraction will not have the same numerical value depending on the mechanism. All the above considerations have been carried out by implicitly considering a “Puddle” mechanism. However, even if the values differ, the trends observed remain valid even when calculations are based on the “Lake” model.

However, if this confirms the robustness of the approach and the understanding of the underlying phenomena, it is necessary to use P' and Csat to refine the criteria for choosing a quinone. Thus, based on the

principle that quinones are rather lipophilic species, it may be relevant to correlate some of the data obtained with the partition constant P (or logP in logarithmic scale). This usually represents the solubility ratio of a substance “i” between two solvents, in this case octanol and water (P = Cᵢ,octanol/Cᵢ,water), and the higher the P value, the more lipophilic the molecule (i.e. logP >0).

$$ P = \frac{C_{Q,octanol}}{C_{Q,water}} \qquad (7) $$

In this context, except once again for BQ (8), a reasonably satisfactory correlation is obtained, not only between P and P', but also for Csat and P (Fig. 11). This suggests that logP is a second relevant parameter for considering the properties of a quinone with regard to its interactions with microalgae. In other terms, LogP could reflect the possible loss of quinone. So low logP values should be preferred because a quinone that is too lipophilic should be avoided, as it will then be mostly lost in membranes and useless for photosynthetic electron harvesting. Conversely, quinones must remain sufficiently lipophilic to be able to cross membranes and access the photosynthetic chain.

## 4. Discussion

The formal standard potential at pH 7 of redox couples involving the quinone form is an essential parameter for predicting the most suitable

<figure><img src="image_16.png" /></figure>

<figure><img src="image_17.png" /><figcaption>Fig. 11. Correlations between P' (A) or Csat (B) with P values in logarithmic scale. This original figure is partially built from data published in Ref. [32].</figcaption></figure>
structure for photosynthetic electron extraction. It leads to a global straightforward relationship towards resulting photocurrents. This type of correlation has already been noted in a recent study of external electron transfer from immobilized *E. coli* bacteria mediated by exogenous quinones [35]. Using carbon paper as a working electrode and amperometry measurements, the authors noticed a linear relationship between the measured current densities and quinone reduction potentials (determined by cyclic voltammetry in aqueous and aprotic media). As already mentioned above, photocurrents recorded from immobilized photosynthetic purple bacteria at carbon paper electrodes were also found to directly depend on quinone reduction potentials (DFT calculations for the Q⁻/Q couple) [31]. Unfortunately, this parameter is necessary but not sufficient, for several reasons. Indeed, it seems to cover several concurrent behaviors, which means that a “mild” value of E° should be considered to date. In fact, its apparent correlation with a toxic effect suggests that a quinone with high oxidizing power will be particularly efficient in diverting electrons from the photosynthetic chain, but also in interacting in undesired ways with other electron transfer chains such as the respiratory chain. In this context, and because the used quinone concentration matters, any “moderation” of the E° value remains imprecise and difficult to predict at this stage.

A second relevant parameter is the quinone partition constant P. Once again, its value seems to have to be “moderated” to avoid too lipophilic quinones being lost in membranes, and less lipophilic quinones being unable to be uptaken. Finally, the same problem arises as for E°, i.e. determining the best intermediate value for logP. Fig. 12 shows the standard potential of the QH₂/Q couple at pH 7 and the logP value for several quinones. Using DMPPBQ (10) and its E° value as the reference quinone giving the most stable photocurrent for a concentration of 100 µmol L⁻¹ and a logP value of 2 (i.e. indirectly corresponding to an intermediate Csat value), a first assessment of the E°/logP couple defining an efficient quinone giving stable performance is obtained.

From these two observations, a quantitative structure activity relationship (QSAR) based on these two parameters can be performed. We considered a similar approach to that used to study phenazine mediated extracellular electron transfer in *Escherichia coli*, namely multivariate linear regression (MLR) modeling [36]. The aim was to find a correlation between the experimental electric current extracted from the mediator as a function of two parameters, i.e. the standard potentials calculated by DFT and polarizability in the corresponding study. From this correlation, a predicted expression between the current and the parameters is established and the resulting current compared to experimental ones. Another MLR treatment was reported for the bioelectrocatalytic glucose oxidation by glucose oxidase (GOx). In that case, after the glucose

oxidation, the active GOx form was recovered through an electron transfer with an added quinone, the resulting hydroquinone form being oxidized at a glassy carbon electrode [37]. From the steady state currents measured by cyclic voltammetry, the authors estimated the corresponding rate constants and established a linear correlation for this parameter with E°(Q/QH₂) and the projected area of the quinone.

In our case, a 3D linear regression can be implemented to model the photocurrent from the standard potential (E°'(QH₂/Q) or E°(Q⁻/Q)) and logP according to:

$$I_{\text{max}} = A + B.E^{\circ} + C.\log P \quad (8)$$

With Imax in µA and E° in mV vs SHE.

Fittings considering all our data in line with nine quinones (DCBQs, PPPBQ, DMBQs, tBu₂BQs, DQ, DMPPBQ i.e. 1, 2, 3, 4, 5, 6, 7, 9 and 10) gave the following results (Table 1):

The comparison between experimental photocurrents and those predicted by the two models is therefore globally satisfactory (Fig. 13). However, it should be pointed out that several quinones giving poor results, namely BQ, NBQ and DCMorBQ (8, 11 and 12), were discarded from the data treatment. This probably stems from the side actions of these three quinones, which may either not contribute to photocurrent or lower its magnitude. BQ (8), for example, is an unsubstituted quinone and therefore perfectly capable of reacting with nucleophiles (vide infra) in a cross-linking process [38]. NBQ (11) could also be involved in a similar reactivity, but has also been suggested as strongly capable of binding to PSII without efficient electron transfer, giving it an inhibitory effect [33]. Finally DCMorBQ (12), due to its morpholine substituents (with donor nitrogen atoms) can bind irreversibly with the QB pocket, leading to the same inhibitory behavior [30].

It is important to point out that this MLR approach to establishing a structure-activity relationship does not provide the same physicochemical basis as those developed in our previous work to understand and model the percentage of open centers as a function of quinone concentration, [33] the modeling of the shape of experimental photocurrents [29,39] or the evolution of NPQ relative to that of the photocurrent [40,41]. It is therefore only a first approach which does not take into account, for example, the instability of photocurrents.

Unfortunately, as evidenced by exclusion of three quinones from the fittings, the design of the optimal quinone is not restricted to the question of quantifying a compromise for the values of E° and logP. Here is a list, probably not comprehensive, of issues that need to be addressed in the future.

1) Which redox couple should be considered for E°? The studies reported for *Chlamydomonas reinhardtii* suggest that both Q⁻/Q and QH₂/Q pairs could be taken into account, although it is not clear which is the most relevant to describe the given quinone. Other studies on photosynthetic purple bacteria show that this may not be the case and that the semiquinone/quinone pair may be the most relevant [31]. This ambiguity needs to be clarified.

2) Which partition constants? Even for the quinone form, there are several ways of accessing the logP value, either theoretically (Abraham's equation taking into account molecular volume, H-bonding, polarity, polarizability or increments/fragments method), experimentally (distribution measurements between octanol and water volumes by UV-Vis or HPLC and even with fluorescence from nanoparticles/membranes assemblies) or by a combination of both (neural networks where a comparison for a given structure to a pool

<table><caption>**Table 1**

Parameters of Eq. (8) giving the best results to predict the photocurrent resulting from the micro-algae/quinone mixture.</caption><thead><tr><th>Standard potential used in the fittings</th><th>A (µA)</th><th>B (µA mV<sup>-1</sup>)</th><th>C (µA)</th><th>R<sup>2</sup></th></tr></thead><tbody><tr><td>E°'(QH<sub>2</sub>/Q)</td><td>7.937</td><td>7.16 10<sup>-2</sup></td><td>-4.402</td><td>0.97</td></tr><tr><td>E°(Q<sup>-</sup>/Q)</td><td>21.31</td><td>3.58 10<sup>-2</sup></td><td>-3.533</td><td>0.92</td></tr></tbody></table>

<figure><img src="image_18.png" /><figcaption>**Fig. 12.** E°-logP mapping for the quinones considered in this work.</figcaption></figure>
<figure><img src="image_19.png" /></figure>

<figure><img src="image_20.png" /><figcaption>**Fig. 13.** Comparison between predicted currents from MLR approach with (A) E°(QH₂/Q) or (B) E°(Q⁻/Q) as a variable in the modeling equation. Three quinones (8, 9 and 12) are not included in the linear regression.</figcaption></figure>

of experimental values defines a calibration). Which gives the most reliable values (and for which octanol is not necessarily fully indicative of a lipid membrane)? Of course, these questions become particularly relevant for the hydroquinone form resulting from electron extraction, which must then be released by the microalgae to the collecting electrode. In this case, the question of the pH effect and therefore the distribution constant is an additional complication to an already far from easy problem.

3) As a consequence, the main challenge is undoubtedly to elucidate the mechanisms of quinone poisoning in parallel with photosynthetic electron harvesting. Several hypotheses can be proposed:

a) **the production of reactive oxygen species (ROS)** [42,43]. In this case, the reduced form of the quinone, i.e. semiquinone Q⁻ or hydroquinone QH₂, could react (directly or undirectly) with O₂ to generate superoxide anion O₂⁻ (the precursor of many ROS) or H₂O₂ respectively (Scheme 5).

From a thermodynamic point of view, such reactions producing O₂⁻ and ROS should be rather unfavorable because formal potentials for redox couples involving O₂ (E°(H₂O₂/O₂) = 260 mV at pH 7 and E°(O₂/O₂) ~ -180 mV vs SHE) are lower than those for diverting and oxidizing quinones (E°(QH₂/Q) at pH 7 ~ 270-330 mV and E°(Q⁻/Q) ~ 80-230 mV). However, the superoxide anion can be rapidly formed, even if its formation remains thermodynamically unfavored, and in small quantities can still generate ROS [44].

b) a reaction of the quinone form with nucleophiles via a so-called **Michael reaction** (Scheme 5), which both consumes the quinone and subsequently alters metabolism as for the case of BQ (8) [42,44]. This reaction could perhaps be restrained if the quinone is tetra-substituted and/or the substituents are bulky.

c) **Other undesirable effects of quinones.** Recent measurements (fluorescence, absorbance, O₂ content) suggest that quinones may trigger cyclic electron transfer (instead of the conventional linear transfer) in the photosynthetic chain, or even interfere with the respiratory chain [45].

Another hypothesis is that the quinone itself induces toxicity through its mediating activity. In other words, it would be the short-circuiting and interruption of the endogenous electron flow by the quinone that would be indirectly responsible for the performance impairment. As already mentioned above, the question of quinone stability over the experiment duration could be important to consider. Quinones surely can degrade through their poisoning effect. In this case, their side reactions within the algae could both alter the metabolism of the photosynthetic organism and effectively reduce the amount of quinones available for electron extraction. Furthermore, the quinone "natural"

<figure><img src="image_21.png" /><figcaption>**Scheme 5.** Possible side reactions involving quinones in parallel to electron harvesting.</figcaption></figure>
decomposition could be also considered, possibly through a photo-catalyzed Michael reaction in presence of water, that would make it intrinsically less effective as its concentration decreases. Points related to the excessive oxidizing activity of quinones or their chemical instability were thus recently suggested over long periods (80 h) in the case of *Synechocystis* sp. PCC 6803 in the presence of 1,4-benzoquinone (BQ, 8; decomposition rate estimated at 9 µmol L⁻¹ h⁻¹) [46].

In one way or another, these three points mean having to consider the size, number and nature of the quinone's substituents and its steric hindrance by means of molecular volume. Beyond these questions (and also the effect of quinone concentration), we could further add the aspect of time and the development of future studies over hours and days to study a population of microalgae that could adapt and endure an environment supplemented with quinones.

## 5. Conclusion

In order to capture electron flow along the photosynthetic chain, the strategy of using exogenous quinones as redox mediators is particularly promising. Indeed, these structures have the advantage of being neutral in both oxidized and reduced forms, giving them a favorable balance between lipophilic and hydrophilic properties, enabling them to cross cell membranes and not remain totally trapped on one side or the other.

The relevance of this approach is demonstrated by the numerous studies on different photosynthetic targets reporting photocurrents. However, this strategy seems to have reached a limit at this stage, particularly in view of the difficulties encountered in properly rationalizing the quinone effect. While the redox potential of the couples involved is undoubtedly a key consideration, other points remain to be clarified. In this article, we show that the partition coefficient can be an important factor in establishing a quantitative structure-activity relationship. However, it appears that this new parameter cannot by itself summarize the numerous side effects of quinones in this context, and that further analysis and development will be necessary. In other words, new parameters would be necessary to go beyond the maximum photocurrent and to include how stable is the electricity production from the quinone/photosynthetic target mixture.

### 5.1. Experimental part

The experimental data discussed in this paper come from previous articles by our research group (references are given in the text). They are either presented in a different way or analyzed and processed in a new approach to support some previously suggested or newly proposed trends. All the measurements were performed in into Tris-minimal medium (TAP = Tris base (20 mmol L⁻¹), NH₄Cl (7 mmol L⁻¹), MgSO₄ (0.83 mmol L⁻¹), CaCl₂ (0.45 mmol L⁻¹), K₂HPO₄ (1.65 mmol L⁻¹), KH₂PO₄ (1.05 mmol L⁻¹)). Error bars correspond to s.e.m. (standard error of the mean) deduced from at least 3 measurements under the same experimental conditions. Advanced Chemistry Development Software (ACD/Labs - PhysChem Suite) has been used to calculate all theoretical modeling for LogP values of each quinone. All plots, fittings and statistical analyses were performed using SIGMA Plot 10.0 software (Systat Software Inc., Richmond, CA, USA).

## CRediT authorship contribution statement

**Adnan Sayegh:** Methodology, Investigation, Formal analysis, Data curation, Conceptualization.
**Guillaume Longatte:** Methodology, Investigation, Formal analysis, Data curation, Conceptualization.
**Léna Beauzamy:** Investigation, Formal analysis.
**Eric Labbé:** Writing – review & editing, Investigation, Formal analysis.
**Olivier Buriez:** Writing – review & editing, Investigation, Formal analysis.
**Jérôme Delacotte:** Writing – review & editing, Methodology, Formal analysis.
**Manon Guille-Collignon:** Writing – review & editing, Supervision, Methodology, Investigation.
**Frédéric Lemaître:** Conceptualization, Data

curation, Formal analysis, Investigation, Methodology, Supervision, Validation, Writing – original draft, Writing – review & editing.

## Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

## Acknowledgements

This work has been supported in part by CNRS (UMR 8228 and UMR 7141), Ecole Normale Supérieure, French Ministry of Research, Faculté des Sciences et Ingénierie - Sorbonne Université and the "Initiative d'Excellence" program from the French State (Grant "DYNAMO", ANR-11-LABX-0011-01). We warmly thank Fabrice Rappaport, Francis-André Wollman, Benjamin Bailleul and Pierre Joliot for all their fruitful exchanges and contributions throughout this long-term project.

## Data availability

Data will be made available on request.

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